Download Ecology of aerobic anoxygenic phototrophs in aquatic environments

FEMS Microbiology Reviews, fuv032, 39, 2015, 854–870 doi: 10.1093/femsre/fuv032 Advance Access Publication Date: 2 July 2015 Review Article REVIEW ARTICLE Ecology of aerobic anoxygenic phototrophs in aquatic environments Michal Koblı́žek1,2,∗ 1 Institute of Microbiology CAS, Center Algatech, 379 81 Třeboň, Czech Republic and 2 Faculty of Science, University of South Bohemia, Branišovská 31, 370 05 České Budějovice, Czech Republic ∗ Corresponding author: Institute of Microbiology CAS, Center Algatech, 379 81 Třeboň, Czech Republic. Tel: +420-384340432; Fax: +420-384340415; E-mail: [email protected] One sentence summary: The review covers current knowledge about the distribution and diversity of aerobic anoxygenic phototrophs in aquatic environments and their role in the aquatic food webs and the microbial loop. Editor: Corina Brussaard ABSTRACT Recognition of the environmental role of photoheterotrophic bacteria has been one of the main themes of aquatic microbiology over the last 15 years. Aside from cyanobacteria and proteorhodopsin-containing bacteria, aerobic anoxygenic phototrophic (AAP) bacteria are the third most numerous group of phototrophic prokaryotes in the ocean. This functional group represents a diverse assembly of species which taxonomically belong to various subgroups of Alpha-, Beta- and Gammaproteobacteria. AAP bacteria are facultative photoheterotrophs which use bacteriochlorophyll-containing reaction centers to harvest light energy. The light-derived energy increases their bacterial growth efficiency, which provides a competitive advantage over heterotrophic species. Thanks to their enzymatic machinery AAP bacteria are active, rapidly growing organisms which contribute significantly to the recycling of organic matter. This chapter summarizes the current knowledge of the ecology of AAP bacteria in aquatic environments, implying their specific role in the microbial loop. Keywords: photoheterotrophs; microbial loop; aquatic food webs; bacteriochlorophyll; bacterial growth INTRODUCTION Phototrophic bacteria are one of the oldest life forms on Earth. The ability to use light represents a major evolutionary innovation which secured a continuous supply of energy to sustain life on this planet. While oxygenic phototrophs—cyanobacteria and algae—provide most of the fixed carbon in the ocean, there exists a broad phylogenetic spectrum of anoxygenic (non-evolving oxygen) phototrophic bacteria containing bacteriochlorophyll (BChl). Anoxygenic phototrophs are divided into six major phyla—Proteobacteria (purple photosynthetic bacteria), Chlorobi (green sulfur bacteria), Chloroflexi (green non-sulfur bacteria), Firmicutes (heliobacteria), Acidobacteria and Gemmatimonadetes (Fig. 1). Each of these lineages contain a unique photosynthetic apparatus differing in the light-harvesting complex architecture, pigment composition and function of their reaction centers (Hohmann-Marriott and Blankenship 2011; Zeng et al. 2014). In addition, there are a large number of phototrophic bacteria that contain special proteins called proteorhodopsins (Béjà et al. 2000). The proteorhodopsin-containing bacteria are highly abundant in both marine and freshwater environments (Finkel, Béjà and Belkin 2013), but these organisms will not be covered here. Anoxygenic phototrophs probably evolved during the Archean period some 3 Gyr ago, when the Earth’s atmosphere was largely anoxic. Therefore, many anoxygenic phototrophs evolved as anaerobic species, which till now grow and photosynthesize only under anoxic conditions. At the beginning of the Proterozoic era (2.4–2.0 Gyr ago), oxygen produced by cyanobacteria started to gradually oxygenate the Earth’s Received: 14 January 2015; Accepted: 5 June 2015 C FEMS 2015. All rights reserved. For permissions, please e-mail: [email protected] 854 Koblı́žek s rmu ter ia tro Ni flex oid et es Ba cte r i pro s lta ale De ibrion fov sul eae De urellac Desulf lonproteobacteria a oro ia ter ac b teo ir sp Chl eres Fibrobact tes nade ac mo mati Gem ob The us− occ noc tin Planctomycetes C Lentis hlamydiae ph Ver aerae r Ch ucomicr lor obia ob Dei Ac 855 i Epsi Firmicutes Acidobacteria ae s Archaea ae og ot m ia te ae er ter ch Th iro ria cte ba teo ro ap ph Al aproteobacteria Beta- and Gamm 0.1 Ch Def rysiogen errib e acte tes res Fu so ba Cy ct an er ob ia ac Sp a teri bac o f l u es des tet mo s r i e g r Th ne Sy Aquific Figure 1. 16S rRNA phylogenetic tree of main phyla within domain Bacteria. AAP bacteria belong to phylum Proteobacteria (marked in red). The other phyla containing chlorophototrophic species are shown in orange. atmosphere, reaching the present concentrations approximately 500 Myr ago (Bekker et al. 2004; Holland 2006). Under the new conditions, many anaerobic species probably disappeared or retreated to the remaining anoxic habitats. However, some groups of purple non-sulfur bacteria adapted to the new aerobic conditions and gradually embarked on an aerobic life style (Koblı́žek et al. 2013). DISCOVERY OF AEROBIC ANOXYGENIC PHOTOTROPHS The first aerobic species of anoxygenic phototrophs were discovered by Tsuneo Shiba (see Fig. 1, Supporting Information) and Keiji Harashima in the 1970s (Harashima, Shiba and Murata 1989). They isolated several pigmented aerobic strains from the surface of the green seaweed Enteromorpha linza collected at Aburatsubo Inlet, Miura Peninsula near Tokyo. During the thin layer chromatography analyses of the pigment composition they noticed a blue spot, which turned out to be BChl a. This finding came as a surprise since BChl a had, until then, only been reported in photosynthetic bacteria grown under anaerobic or semiaerobic conditions. One of the first isolates, the orange strain OCh 101 (Harashima et al. 1978; Shiba, Simidu and Taga 1979a), was later formally described as Erythrobacter longus establishing the first genus containing aerobic photosynthetic bacteria (Shiba and Shimidu 1982). Another organism isolated from E. linza was a pink bacterium originally called Erythrobacter sp. OCh 114. This strain, later reclassified as Roseobacter denitrificans, established (together with R. litoralis) the second new genus— Roseobacter (Shiba 1991). Subsequently, many BChl a-containing strains were isolated from various seaweeds, algal mats, stromatolites, sand or coastal waters (Shiba, Simidu and Taga 1979b; Shiba et al. 1991; Nishimura et al. 1994). All these strains contained BChl a as a main light-harvesting pigment, but in contrast to purple non-sulfur photosynthetic bacteria, they were obligate aerobes, which grew and produced BChl a under fully oxic conditions. The newly established group of phototrophic organisms was originally named aerobic photosynthetic bacteria (Harashima, Shiba and Murata 1989), but later the terminology settled on the term aerobic anoxygenic phototrophic (AAP) bacteria (Yurkov and Beatty 1998a) or aerobic anoxygenic phototrophs (Yurkov and Csotonyi 2009). During the last two decades of the 20th century, AAP bacteria remained a domain of classical microbiologists who kept describing novel AAP genera from various aquatic habitats (Fig. 2, Supporting Information). The first freshwater AAP species were isolated by Yurkov and Gorlenko from the surface of alkaline cyanobacterial mats growing in and around an alkaline thermal spring near Lake Baikal (Yurkov and Gorlenko 1990, 1992; Yurkov et al. 1994). Later, acidophilic species of the genus Acidobacterium containing a zinc form of BChl a were isolated from mine drainage water (Wichlacz, Unz and Langworthy 1986; Wakao et al. 1993; Hiraishi and Shimada 2001). Several Roseobacterrelated AAP species were isolated from saline lake Clifton in 856 FEMS Microbiology Reviews, 2015, Vol. 39, No. 6 Figure 2. Colorful cultures of AAP bacteria. From left to right: Roseobacter litoralis, Roseococcus thiosulfatophilus, Erythrobacter longus and Sphingomonas sp. AAP2. UTILIZATION OF LIGHT ENERGY One of the issues discussed from the very beginning was the photosynthetic competence of newly isolated organisms. All AAP species contain photosynthetic complexes with BChl a as the main light-harvesting pigment. However, their BChl a content is significantly lower when compared to purple non-sulfur bacteria (Harashima et al. 1980; Shiba 1987; Biebl and WagnerDöbler 2006; Koblı́žek et al. 2010; Fig. 3, Supporting Information). Interestingly, BChl a synthesis in most AAP species is inhibited by light (Shiba 1987; Iba and Takamiya 1989). The reason for this physiological feature is probably the need to avoid the simultaneous presence of light, BChl a biosynthesis intermediates and oxygen, which could lead to the production of harmful reactive oxygen species (Nishimura et al. 1996). The visible pigmentation of AAP species is usually orange, red, pink, brown or yellow due to the presence of various carotenoids (see Fig. 2). The carotenoid composition differs among various AAP groups (Yurkov and Csotonyi 2009; Zheng et al. 2013). Carotenoids serve as auxiliary pigments which extend absorption to the blue-green part of the spectrum (see Fig. 3). This is important in aquatic habitats, where the UV-A and near infrared part of the spectrum available for BChl a are rapidly absorbed by the water and only the blue-green part of the solar spectrum penetrates into the deeper parts of the water column. The excitation energy captured by the carotenoids is transferred within picoseconds to the BChl a molecules (Šlouf et al. 2013) and used for primary charge separation in the reaction center. In addition, some AAP species (i.e. genera belonging to Rhodospirillales and Sphingomonadales) contain large amounts of carotenoids, which are not bound to photosynthetic complexes (Takaichi et al. 1991; Yurkov, Gad’on and Drews 1993). Erythrobacter sp. NAP1 Dinoroseobacter shibae Congregibacter litoralis Absorbance [rel. units] West Australia (Shiba et al. 1991) and lake Ekho in Antarctica (Labrenz et al. 1999, 2000). The first AAP bacterium belonging to the Betaproteobacteria Roseateles depolymerans was isolated by Suyama et al. (1999) from Hanamuro River in Japan. The classical culture work on AAP bacteria has been excellently reviewed in the following references (Yurkov and Beatty 1998a; Yurkov and Csotonyi 2009; Yurkov and Hughes 2013). 300 U.V. 400 500 600 700 800 900 N.I.R Wavelength [nm] Figure 3. In vivo absorption spectra of AAP species recorded using Shimadzu UV3000. The cells were resuspended in 70% glycerol to reduce scattering. Notice the presence of peripheral light-harvesting complexes in D. shibae absorbing at 804 nm and the large amount of non-photosynthetic carotenoids in Erythrobacter sp. NAP1. These carotenoids do not have any light-harvesting function and probably only serve for photoprotection. The functionality of the photosynthetic reaction centers in AAP bacteria has been demonstrated by spectroscopic (Harashima et al. 1987; Stadnichuk et al. 2009; Rathgeber et al. 2012) and IR kinetic fluorescence measurements (Kolber et al. 2001; Sato-Takabe, Hamasaki and Suzuki 2012, 2014). On the other hand, AAP bacteria are unable to grow photoautotrophically as they lack carbon fixation pathways (Fuchs et al. 2007; Swingley et al. 2007; Koblı́žek et al. 2011). (The weak light-mediated CO2 incorporation observed in some AAP species (Shiba 1984; Kishimoto 1995; Koblı́žek et al. 2003) originates from anaplerotic carboxylation reactions connected to the citric acid cycle (Tang et al. 2009). The anaplerotic carboxylation may contribute 0.6–11% of Koblı́žek total cellular carbon (Hauruseu and Koblı́žek 2012). The obligatory requirement for organic substrates and the ability to grow in the dark (Shioi 1986; Yurkov et al. 1999; Koblı́žek et al. 2003; Spring et al. 2013) indicate that AAP bacteria utilize light energy as an additional source of energy for their mostly heterotrophic metabolism (Harashima et al. 1987). Light exposure of AAP cells inhibits respiration (Harashima et al. 1987; Koblı́žek et al. 2010) and increases their cellular ATP concentration (Okamura et al. 1986; Candela, Zaccherini and Zannoni 2001). This documents that AAP bacteria are able to replace a large part of oxidative phosphorylation with photophosphorylation. The light-derived energy may cover a large portion of cellular metabolic needs. It has been demonstrated that light exposure increases the survival of AAP cells under starvation (Shiba 1984; Soora and Cypionka 2013). Utilization of light energy also saves organic substrates, which would otherwise have to be respired. Indeed, it has been repeatedly shown that exposure of AAP bacteria to light increases biomass yields (Shioi 1986; Yurkov and van Gemerden 1993; Biebl and Wagner-Döbler 2006; Spring et al. 2009). Experiments using chemostat cultures of Erythrobacter sp. NAP1 and Roseobacter sp. COL2P grown on defined carbon sources show that under light–dark cycles these bacteria accumulate 25–110% more carbon when compared to cultures grown in the dark (Hauruseu and Koblı́žek 2012). In summary, AAP bacteria can be classified as facultative photoheterotrophs—they can grow in the dark on organic carbon substrates; on the other hand, they are able to derive a significant portion of their energy requirements from light (Hauruseu and Koblı́žek 2012; Kirchman and Hanson 2013). DISCOVERY OF AAP BACTERIA IN THE OCEAN In spite of the accumulating knowledge regarding the diversity and physiology of AAP bacteria, nothing was known about the distribution or the role of AAP bacteria in the natural environment. This situation changed dramatically in 1998, when Vladimir V. Yurkov and his colleagues reported the isolation of a novel AAP bacterium Citromicrobium bathyomarinum. This organism was collected from black smoker plume waters of the Juan de Fuca Ridge (Yurkov and Beatty 1998b; Yurkov et al. 1999). It was speculated that hydrothermal vents emanating infrared radiation and supplying an ample amount of reduced metals or sulfides may have represented an environment where the first anoxygenic phototrophs originally evolved (Nisbet, Cann and Van Dover 1995). This news caught the attention of marine biologists Falkowski and Kolber who then decided to explore the presence of novel species directly in the vicinity of the hydrothermal vents. They modified their fast repetition rate fluorometer, originally developed for phytoplankton measurements, extending its sensitivity to the infrared region. The measurements were conducted during the cruise exploring the hydrothermal vents at East Pacific Rise in the spring of 1999 and the samples were collected using the deep-ocean submersible Alvin (DSV-2). Unfortunately, the new instrument failed to record any BChl a signals in the water samples collected around the vents. After several futile attempts, Kolber decided to test the instrument with samples collected from the surface. Unexpectedly, the surface samples revealed weak infrared fluorescence transients, signaling the presence of BChl-containing organisms. The infrared fluorescence was then recorded along a more than 1000 km long transect, demonstrating that the observed signals were distinct from phytoplankton emission and that they indeed originated 857 from AAP bacteria (Kolber et al. 2000). The article of Kolber et al. (2000) together with a study describing proteorhodopsincontaining bacteria (Béjà et al. 2000) immediately attracted the attention of marine microbiologists. (Interestingly, by coincidence these articles describing the two main groups of marine photoheterotrophs were published almost in the same moment. The article of Kolber et al. published in Nature on 14 September 2000 preceeded the study of Béjà et al. (2000) in Science just by 1 day.) The reports of large amounts of photoheterotrophic organisms in the ocean (Eiler 2006; Béjà and Suzuki 2008; Zubkov 2009) challenged the classical view of marine bacteria as heterotrophic organisms fully dependent on recycling dissolved organic matter (DOM) produced by photoautotrophic phytoplankton. A controversy surrounded the first reports regarding AAP abundance. In the follow-up study using infrared epifluorescence microscopy, Kolber et al. (2001) found that AAP bacteria made up 11% of total bacteria in the North East Pacific. These reports were questioned by Schwalbach and Fuhrman (2005), who reported that the fraction of AAP bacteria in the San Pedro Channel in California was much lower, on average 1.66% of total bacteria. Using an alternative quantification by qPCR, the same authors found that AAP bacteria may represent 0.01– 18% of total bacteria in various marine environments (Schwalbach and Fuhrman 2005). Similar criticism was raised by Goericke (2002) who based on the HPLC analyses of BChl a concentration off the shores of California (2–41 ng L−1 ) asserted that anoxygenic photosynthesis in the ocean may not be significant. Following investigations calmed down the initial issues documenting that, despite large differences, AAP bacteria on average constitute typically 1–7% of total prokaryotes in the oligotrophic areas of the oceans. In shelf seas or river estuaries, AAP bacteria may represent 2–15% of total prokaryotes (see Table 1). These numbers were also confirmed by an independent qPCR enumeration (Du et al. 2006) as well as by an analysis of Venter’s metagenomic dataset (Global Ocean Sampling Expedition I), which documented that AAP bacteria made up 1–10% of total prokaryotes in the surface ocean (Yutin et al. 2007). DIVERSITY OF MARINE AAP BACTERIA During the first two decades of AAP research, all information on diversity of marine AAP bacteria was gained from culturedependent studies. The first of Shiba’s isolates, strains OCh 101 (Shiba and Shimidu 1982) and OCh 114 (Shiba 1991), established the first two AAP genera Erythrobacter (class Alphaproteobacteria, order Sphingomonadales) and Roseobacter (class Alphaproteobacteria, order Rhodobacterales). Continuing cultivation efforts led to the description of a number of AAP genera belonging to the Roseobacter clade which represents a large environmentally important subgroup of marine bacteria within the order Rhodobacterales (Wagner-Döbler and Biebl 2006; Luo and Moran 2014; Pujalte et al. 2014). Despite the growing number of AAP taxa, culture-dependent studies cannot provide reliable information on species composition and diversity in environmental samples. This problem was overcome with the application of culture-independent molecular techniques. The majority of environmental studies employ the pufM gene (encoding the M subunit of the bacterial reaction center) as a convenient marker for anoxygenic phototrophs harboring type-2 reaction centers. (The first PCR primers for pufM genes were designed by Nagashima et al. (1997) and Achenbach, Carey and Madigan (2001). Most of the later studies use various modifications of these two primer sets (see Table S1, Supporting 858 FEMS Microbiology Reviews, 2015, Vol. 39, No. 6 Table 1. AAP abundance determined in various marine environments using infrared epifluorescence microscopy. Environment Period North East Pacific San Pedro Channel NW Atlantic Sargasso Sea Mid Atlantic Bight North Pacific Gyre Baltic Sea∗ South Pacific Sargasso Sea East China Sea∗ Shelf seas∗ Open Oceans∗ ∗ ∗ North Atlantic Baltic Sea Mediterranean Sea Chesapeake Bay Mediterranean Sea July 2000 Apr–Sept 2002 Oct 2001, Mar 2002 Oct 2001, Mar 2002 Aug 2003 Feb 2004 Sept 2004–Oct 2005 Oct–Dec 2004 May 2006 Apr 2002–Mar 2003 2003–05 2003, 2005–06 May–July 2005 July 2006 Spring 2007 June 2006 Sept 2005, June and Sept 2007, May 2009 June 2008 Summer 2009 2010–11 Mediterranean Sea Western Arctic Ocean Blanes Bay∗ AAP abundance 103 cells mL−1 Fraction of total Prokaryotes Samples References 15–90 n.a. 13–66 7–15 7–150 0.5–67 0–383 5–194 6–19 2.2–79 n.a. n.a. 13–120 8–310 4.4–65 200–800 2.7–87.7 11.3 ± 1.7% 1.66 ± 0.55% 0.8–9.4% 0.8–2.6% 0.8–18% 0–7% 0–11.6%∗ ∗ 0.3–24.4% 1.9–4.3% 0.5–11.6% 4.46 ± 2.41% 1.52 ± 1.30% 1.5–12.9% 1.0–11.1% 1.4–6.5% 2–12% 0.6–11.1% 30 19 16 10 22 30 71 27 12 ∼80 147 135 24 55 18 8 72 Kolber et al. (2001) Schwalbach and Fuhrman (2005) Sieracki et al. (2006) Sieracki et al. (2006) Cottrell, Mannino and Kirchman (2006) Cottrell, Mannino and Kirchman (2006) Mašı́n et al. (2006) Lami et al. (2007) Koblı́žek et al. (2007) Zhang and Jiao (2007) Jiao et al. (2007) Jiao et al. (2007) Michelou, Cottrell and Kirchman (2007) Salka et al. (2008) Lami et al. (2009) Cottrell, Ras and Kirchman (2010) Hojerová et al. (2011) 0.3–35 n.a. 1.12–50.2 0.1–4% 0.1–14.8% 0.2–6.3% 60 n.a. 16 Lamy et al. (2011b) Boeuf et al. (2013) Ferrera et al. (2014) ∗ Seasonal studies. Whole year average 2.37 ± 2.50% (mean ± st.dev.). ∗∗∗ Refers to surface collected open ocean samples. AAP percentage averages in individual oceans were: 3.79 ± 1.72% for the Indian, 1.57 ± 0.68% for the Atlantic and 1.08 ± 0.74% for the Pacific. ∗∗ Information). The first analyses of AAP composition in marine environments were conducted by Béjà et al. (2002) using bacterial artificial chromosome (BAC) libraries constructed from environmental DNA collected from Monterey Bay in California. One of the fosmids (BAC 60D04) contained a complete set of genes encoding bacterial photosynthesis, documenting the presence of Roseobacter-related organisms. Surprisingly, two other fosmids (BAC65D09 and BAC29C02) contained completely novel pufM sequences only distantly related to at that time known organisms. The new sequences were first tentatively ascribed to phototrophic Beta- or Gammaproteobacteria (Béjà et al. 2002). The ambiguous phylogenetic assignment was later clarified after successful isolation of several gammaproteobacterial strains belonging to the NOR5/OM6 cluster, which contained photosynthetic genes related to the originally retrieved sequences (Cho et al. 2007; Fuchs et al. 2007). Some uncertainty remains regarding the composition of AAP communities in various marine habitats. The first pufM clone libraries constructed from Mediterranean and Red Sea waters indicated that the local AAP communities are dominated by members of the Roseobacter clade (Oz et al. 2005) with a smaller proportion of Gammaproteobacteria (Yutin, Suzuki and Béjà 2005). Analysis of Craig Venter’s Global Ocean Sampling metagenomic data indicated that the AAP community in the Atlantic and Pacific Oceans were formed mostly of Roseobacterrelated species and only a small amount of Gammaproteobacteria species (Yutin et al. 2007). Similar results were also obtained in the Baltic Sea, where the local community was dominated by Roseobacter-related pufM sequences with a small contribution of Sphingomonadales and Betaproteobacteria (Salka et al. 2008). In contrast, a combination of IR epifluorescence and FISH analyses documented the majority of AAP cells in the Baltic Sea were Gammaproteobacteria (Mašı́n et al. 2006). The larger proportion of Gammaproteobacteria was also indicated from pufM analyses conducted in the East China Sea and the North Pacific Gyre where more than one half of the sequences were related to Gammaproteobacteria (Hu et al. 2006). Similarly, analyses conducted along a large Mediterranean Sea transect documented that up to 80% of the obtained pufM sequences came from Gammaproteobacteria (Lehours et al. 2010; Jeanthon et al. 2011). The situation in coastal habitats is much more variable. The study conducted in Delaware Estuary documented that the composition of the AAP community was very diverse with its composition changing along the salinity gradient (Waidner and Kirchman 2008). The upper part of the estuary with a salinity of <5 was dominated by Rhodoferax-related AAP species (Betaproteobacteria), while the lower part of the bay with higher salinity was dominated by Gammaproteobacteria. pufM sequences related to Rhodobacterales were distributed throughout the estuary exhibiting some minor seasonal changes (Waidner and Kirchman 2008). A somewhat different situation was observed at the coastal observatory in the Blanes Bay (western Mediterranean Sea). The pyrosequencing analysis of seasonal changes of AAP communities documented that gammaproteobacterial sequences dominated throughout the year except in spring when Roseobacter-related sequences prevailed (Ferrera et al. 2014). Less information is available from polar regions. Diversity of AAP communities in the Chukchi and the Beaufort Sea (western Arctic Ocean) coastal waters seemed to be mostly influenced by riverine inputs (Boeuf et al. 2014). They were mostly composed of Betaproteobacteria and Rhodobacterales; Gammaproteobacteria were not registered (Cottrell and Kirchman 2009). Similar results were also reported by Boeuf et al. (2013) who also registered smaller amount of Sphingomonadales. A somewhat Koblı́žek different composition was also found in sea ice and seawater AAP communities in the Ross Sea near Antarctica, which consisted of various members of order Rhodobacterales whereas Betaproteobacteria were absent (Koh, Phua and Ryan 2011). AAP BACTERIA IN THE INLAND WATERS Freshwaters In contrast to the accumulating information regarding marine AAP bacteria, their freshwater counterparts have received less attention. The first freshwater AAP species Erythrobacter (now Sandaracinobacter) sibiricus and Erythromicrobium (now Erythromonas) ursincola were isolated by Yurkov and Gorlenko (1990, 1992) from the surface of alkaline cyanobacterial mats growing in and alkaline thermal spring nearby Lake Baikal. Later, Porphyrobacter neustonensis was cultured from neuston layers of freshwater lakes in Australia (Fuerst et al. 1993), and Sandarakinorhabdus limnophila was retrieved from the mountain lake Starnberger See in Germany (Gich and Overmann 2006). Similarly to the first marine species, all these isolates belonged to the order Sphingomonadales within Alphaproteobacteria. A completely new AAP species Roseateles depolymerans belonging to Betaproteobacteria was isolated by Suyama et al. (1999) from Hanamuro River in Japan when screening for poly(hexamethylene) carbonatedegrading bacteria. Later, another phototrophic betaproteobacterium HTCC528 was isolated from an oligotrophic Crater lake in Oregon; unfortunately, its physiology has not been tested (Page, Connon and Giovannoni 2004). Culture-independent approaches were first applied by Waidner and Kirchman (2005) using DNA collected from the Delaware River, USA. In their fosmid library, they identified two fragments of bacterial photosynthesis gene clusters. While one originated from a phototrophic betaproteobacterium, the second one was related to the purple non-sulfur bacterium Rhodobacter which documents that phototrophic communities in freshwater systems may be composed of both AAP bacteria and purple non-sulfur species even in oxic environments. The common occurence of AAP bacteria in Swedish lakes was confirmed using bchL clone libraries targeting both oxygenic and anoxygenic species (Eiler et al. 2009). Photosynthesis genes indicating the presence of AAP species were also found in several single-cell genomes collected from freshwater lakes in Maine and Wisconsin (Martinez-Garcia et al. 2011). The systematic survey of AAP abundance in various limnic systems in central Europe revealed that these organisms during summer made up 2–21% of total bacteria in many oligotrophic and mesotrophic lakes (Mašı́n et al. 2008, 2012). Similar numbers (3–22%) were also found in mountain lakes in Tyrol, Austria (Čuperová et al. 2013), Ebro river (5–14%) in Spain (Ruiz-González et al. 2013) or temperate and boreal lakes (1–37%) in Canada (Fauteux et al. 2015). Interestingly, the highest abundances were found in the acidified mountain lakes Plešné and Čertovo in the Šumava Mountains (Czech Rep., 1090 and 1028 m a.s.l.) where AAP bacteria formed, during the summer maximum, more than half of the bacterial biomass (Mašı́n et al. 2008; see Fig. 7). It has been repreatedly found that in temperate freshwater habitats AAP bacterial contributions undergo large seasonal changes oscillating from almost nil in the late winter period to up to 20% during the summer or early autumn maxima (Čuperová et al. 2013; Lew et al. 2015). A large survey of AAP diversity was conducted in eight lakes in the Meckleburg lake district (Germany) by Salka et al. (2011). This analysis documented that most of the pufM sequences in- 859 deed originated from clades which contain AAP species, despite the fact that four lakes also contained smaller fractions of Rhodobacter-related sequences (purple non-sulfur bacteria). The majority of the obtained sequences was related to Betaproteobacterium Rhodoferax fermentans, with a smaller contribution of various subgroups of Alphaproteobacteria (Salka et al. 2011, Fig. 4). AAP bacteria were also surveyed in several mountain lakes in the Tyrolean Alps. A large difference in both abundance, morphology and diversity was observed between lakes located above and below the treeline. While AAP populations inhabiting the lakes at the highest elevation were composed of large rods probably members of Sphingomonadales (Alphaproteobacteria), the lakes under the treeline were inhabited by a variety of smaller morphotypes representing both Alpha- and Betaproteobacteria (Čuperová et al. 2013; Fig. 5). In contrast, a recent study of ultraoligotrophic cold high mountain lakes in Central Pyrenees, Spain, documented that local AAP communities were mostly composed of Betaproteobacteria. Unlike in the Alps, conductivity, pH and nitrate concentration were the main factors influencing the AAP community composition (Caliz and Casamayor 2014). The common theme of all these above-mentioned analyses is the widespread occurence of phototrophic Betaproteobacteria. The recent report of the presence of photosynthesis genes in the genomes of two Limnohabitans species (Zeng et al. 2012) signalizes that the obtained environmental sequences may have originated from similar organisms. Limnohabitans species are a common component of freshwater bacterioplankton in temperate regions, but till recently it was considered to contain only heterotrophic species (Hahn et al. 2010). Saline lakes The presence of AAP bacteria in brackish and saline lakes was first demonstrated by culture-dependent work in Clifton and Heyward lakes, Australia (Shiba et al. 1991); Ekho Lake, Antarctica (Labrenz et al. 1999); Mahoney Lake, Canada (Yurkova et al. 2002); and East German Creek system (Csotonyi et al. 2008). AAP bacteria were reported from Mediterranean coastal lagoons where they made up 0.1–15% of total bacteria (Lamy et al. 2011a). Similar numbers were also found in high altitude saline lakes in Tibet (pH > 9), where AAP bacteria represented between 0.5 and 9% of total prokaryotes (Jiang et al. 2009). The conducted pufM analyses documented that local AAP communities have a similar composition as found earlier in marine environments. Lakes Gahai and Qinghai with higher salinity were dominated by Roseobacter-related species, whereas the brakish lake Erhai was dominated by Gammaproteobacteria (Jiang et al. 2009). One of the main problems of ecological studies on inland lakes is that available IR epifluorescence or pigment analysis techniques are not able to distinguish between various groups of BChl a-containing bacteria, such as purple sulfur, purple nonsulfur bacteria and AAP bacteria. In larger lakes where the oxic epilimnion and anoxic hypolimnion and sediment are physically well separated, it is relatively safe to assume that observed BChl a positive cells are predominantly AAP species, since standard purple bacteria synthesize only minimum amounts of BChl a under aerobic conditions. Shallow, dynamic water bodies such as coastal lagoons (Lamy et al. 2011a) or soda lakes (Medová et al. 2011) represent a much more challenging situation, where anaerobic species may be mixed up from soil or sediment. Here, the separation of different functional groups is impossible without parallel genetic analyses (Tank, Blümel and Imhoff 2011). On the other hand, in many ecological studies, the separation 860 FEMS Microbiology Reviews, 2015, Vol. 39, No. 6 α vim ans ium radiotoler Methylobacter m rubru um hilium crypt m Acidip u i l i1 iphi TA Acid mB biu izo gi ela yrh a p Brad Ful arin dus rhab kino dara Ci San ● ● ■ ■ 92 83 97 ■ 91 ● ■ 99 ■ 99 ■ 99 ■ ■■ 59 ▲ M Ro eth ■ se ylo ate v les ers ■ a de tili po s u lym ni ■ era ver ns sali s Nev skia ■ ■98 ram osa ■ 99 ■ ▲ 78 β limn op h ila tro 9 9 mi Bl crob as iu to m E m on bath ryth yo rob as ur mar acte sin inu r l co m o ng la us 0.2 62 ■ 59 99 53 52 76 51 79 9 9 cl G a m m a p on roteob a cteriu e m HT eB AC env. clone eB CC2080 AC 65D09 99 re 59 99 99 99 95 ▲ ▲▲ 0 Rhodobacterales sp. BS9 e a ib h rs bacte oseo Dinor 99 99 05 var iu deni s TM1 trific 03 ans 5 Roseiba cterium elongatu m cter Ros eoba seo Ro v. d2 5D 99 02 29C AC eB one en ▲ 69 75 47 sp .R im 28 90 . cl 75 env ns ■ ▲ ▲ Mediterranean Sea Coastal lagoon ■ Mecklenburg lake district ● Alpine lakes ▲ 4 D0 60 AC S2 is rii ica us CC rmis eB ens ctic nd ph e ter ifo antar estfold xa otro lon bac gutt v s ale hot . c eo ter alinu nella zia a p nv Ros bac seis Lokta e en fle lfito Ro 99 br oe Su La H 99 De lRiverF L no os06H ■ imno habita n 03 ss ha p. R bit im a 93 γ ■ ■ ■en v. clon ■■Lim e 65 Congregibacter litoralis ▲ ▲ 98 ▲ 9 bra is 9 a ru tens▲ e i l Ha s syl hilu inip m Lu 62 5 7 81 67 71 ■ ■ 50 β ● P ▲ lan kt om ar in a te m pe ra ta ▲ Roseobacter clade Figure 4. Molecular phylogenetic analysis of partial pufM aminoacid sequences (∼220 aminoacid). The sequences for Mediterranean Sea were obtained from Oz et al. (2005), the Baltic Sea coastal lagoon from Tank, Blümel and Imhoff (2011), freshwater lakes in northen Germany from Salka et al. (2011) and from Alpine lakes in Austria from Čuperová et al. (2013). In addition, the tree includes environmental pufM sequences identified in fosmid libraries published by Béjà et al. (2002), Waidner and Kirchman (2005) and Oz et al. (2005). The phylogeny was inferred by using the maximum likelihood method using the LG evolution model. The tree with the highest log likelihood (−11297.4615) is shown. A discrete Gamma distribution was used to model evolutionary rate differences among sites (five categories (+G, parameter = 0.8231)). The rate variation model allowed for some sites to be evolutionarily invariable ([+I], 11.7036% sites). The tree is drawn to scale, with branch lengths measured in the number of substitutions per site. All positions containing gaps and missing data were eliminated. Only bootstrap values higher than 50 are shown. Koblı́žek 861 Figure 5. Various AAP morphotypes observed in fresh waters (Čuperová et al. 2013). of functional groups may not be necessary, and one may report the observed organisms simply as purple phototrophic bacteria or anoxygenic phototrophs without specifying their physiology. NEW DEFINITION OF AAP BACTERIA The original definition of AAP bacteria as organisms was based on the first obtained isolates namely Erythrobacter and Roseobacter species. The AAP bacteria are defined as aerobic species which synthesize BChl a and conduct photosynthesis under aerobic conditions. The increasing knowledge on the ecology, physiology and genomic of these organisms urges for an update of the current definition. In many freshwater habitats, we encounter species belonging to phototrophic methylotrophs (i.e. genus Methylobacterium) or aerobic phototrophic rhizobia (i.e. genus Bradyrhizobium). These organisms are typically found in soils, associated with vegetation (Atamna-Ismaeel et al. 2012) or plant roots (Sato 1978; Fleischman and Kramer 1998). The relationship of these two groups to AAP bacteria is a matter of dispute. While Shiba and Harashima included chapters about BChl a-containing facultative methylotrophs in their book ‘Aerobic Photosynthetic Bacteria’ (Harashima, Shiba and Murata 1989), Yurkov and Csotonyi (2009) excluded these two subgroups from AAP bacteria. In spite of some subtle differences, both phototrophic methylotrophs and phototrophic rhizobia share the same basic physiology with standard AAP bacteria (Fleischman and Kramer 1998). Both groups are mostly aerobic species, which synthetize BChl a and perform photosynthesis under aerobic conditions. Moreover, laboratory experiments with Bradyrhizobium sp. BTAi showed that photosynthetic electron transport in this organism is oxygen dependent, (similarly to Roseobacter denitrificans) and cannot be conducted under anaerobic conditions (Kramer, Kanazawa and Fleischman 1997). Another source of uncertainty are species which contain photosynthetic genes, but express no or only a minimum amount of BChl a under laboratory conditions. Many such species were originally considered heterotrophic, and the presence of photosynthesis genes was identified only after full genome sequencing. A typical example of such an organism is Planktomarina temperata representing an abundant RCA lineage of the Roseobacter cluster (Selje, Simon and Brinkhoff 2004). This bacterium contains functional photosynthetic genes but expresses only miniscule amounts of the pigment under laboratory conditions (Giebel et al. 2013). However, recent metatranscriptomic analysis documented that these organisms express its photosynthetic genes under in situ condition (Voget et al. 2015). A similar situation was found among the representatives of the freshwater genus Limnohabitans, which was originally established for heterotrophic species. While pigment expression has not been observed under laboratory conditions, the full genome sequencing documented the presence of the complete photosynthesis gene clusters among two Limnohabitans sp. strains (Zeng et al. 2012). An example of another cryptic phototroph is the common neuston bacterium Nevskia ramosa. This organism was already described in the 19th century (Famintzin et al. 1892), but the presence of photosynthetic genes was revealed only after its full genome sequencing in 2013. These organisms do not fit the strict definition of an AAP bacterium since they do not synthesize BChl a under tested laboratory conditions. They presumably do express photosynthetic apparatus under some specific environmental in situ conditions, but the information on their pigment expression under natural conditions is so far missing. FEMS Microbiology Reviews, 2015, Vol. 39, No. 6 Facing all these uncertainties, I suggest to expand the term AAP bacteria to all mostly aerobic species, which express (at least facultatively) purple bacterial photosynthetic reaction centers under fully oxic in situ conditions. An alternative would be the term aerobic BChl-containing bacteria (introduced by JF Imhoff), which may serve as an umbrella group for AAP bacteria (sensu stricto), phototrophic methylotrophs, phototrophic rhizobia and all the other mostly aerobic photoheterotrophs without indicating any specific physiology, ecology or taxonomical classification. 5 3 2 1 INFLUENCE OF THE MAIN ENVIRONMENTAL FACTORS 0 0.01 0.1 1 10 100 -3 Chlorophyll a [mg m ] 12 AAP bacteria [%] The ecology of AAP bacteria is not completely understood. In his pioneering paper, Kolber et al. (2000) speculated that the ability to utilize light may be especially beneficial in nutrient-poor marine environments. The hypothesis was repeatedly disproved based on the data documenting that AAP bacteria are more numerous in more productive regions (Schwalbach and Fuhrman 2005; Sieracki et al. 2006; Jiao et al. 2007; Lamy et al. 2011b). In part, the controversy was caused by the different backgrounds of the individual research groups. Phytoplankton ecologist Kolber routinely used normalization per chlorophyll which resulted in higher bacteriochlorophyll a/chlorophyll a ratios in oligotrophic areas (Kolber et al. 2000) and smaller ratios in meso and eutrophic regions. The same trends were observed on the pigment data from the Black and Baltic Seas (Koblı́žek et al. 2005; Koblı́žek, Falkowski and Kolber 2006; see Fig. 6 upper panel) and the global dataset by Jiao, Zhang and Hong (2010). In contrast, normalization of the AAP abundance per total bacteria (DAPI) used by microbiologists frequently revealed higher proportions of AAP bacteria in more productive marine regions or coastal waters (see Table 1 and Fig. 6 lower panel) documenting that AAP bacteria prefer more productive habitats. Most of the surveys of AAP bacteria in marine environments have shown a positive correlation between AAP abundance and chlorophyll concentration (Jiao et al. 2007; Hojerová et al. 2011; Ritchie and Johnson 2012). A similar relationship was also documented for saline (Medová et al. 2011) and freshwater lakes (Mašı́n et al. 2012). However, it is not clear whether the relationship reflects the direct association with primary producers or the same dependence on limiting nutrients such as phosphate or nitrogen. Indeed, the common relationship of AAP abundance, total bacteria, chlorophyll and total phosphorus was documented in freshwater lakes (Mašı́n et al. 2012; Fauteux et al. 2015). Surprisingly, the most enigmatic factor in the AAP ecology is the influence of light. While the positive influence of light has been repeatedly demonstrated in laboratory experiments, its effect on natural AAP communities remains inconclusive. A DNA fingerprinting study indicated a strong influence of light over a large part of the marine bacterial community in the North Pacific Ocean (Van Mooy, Devol and Keil 2004). In contrast, experiments conducted in San Pedro Channel (California) did not show any effect of light on bacterioplankton structure (Schwalbach, Brown and Fuhrman 2005). Ambiguous results were also obtained in experiments directly analysing natural AAP assemblages. While AAP bacteria in Chesapeake Bay had higher leucine incorporation activities when compared to average bacteria, no effect was found between light and dark treatments (Stegman, Cottrell and Kirchman 2014). Also, in our experiments conducted in freshwater lakes we failed to observe any clear stimulation of AAP growth by light. It seems that the effect of light on natural AAP Atlantic Ocean Baltic Sea Black Sea Mediterranean Sea 4 BChl a/Chl a ratio [%] 862 9 6 3 0 0.01 0.1 1 10 100 Chlorophyll a [mg m -3 ] Figure 6. Upper panel: bacteriochlorophyll a/chlorophyll a ratios determined in the Baltic Sea (Koblı́žek et al. 2005), Black Sea (Koblı́žek, Falkowski and Kolber 2006), Mediterranean Sea (Koblı́žek, Falkowski and Kolber 2006; Lami et al. 2009; Hojerová et al. 2011) and the Atlantic Ocean (Koblı́žek et al. 2007). Bacteriochlorophyll was estimated from IR fluorescence measurements, chlorophyll in pigment extracts. Lower panel: relative AAP abundances (percentage of total DAPI counts) determined by IR epifluorescence microscopy in the Baltic Sea (Mašı́n et al. 2006), Sargasso Sea (Koblı́žek et al. 2007) and the Mediterranean Sea (Hojerová et al. 2011). consortia is probably too small to be easily recognized during short experiments. On the other hand, AAP bacteria are typically observed in the euphotic zones of the oceans or lakes (see Fig. 7). Below the euphotic zone, AAP numbers fall to nil. A positive effect of light was also be documented from seasonal studies conducted in the Mediterranean coastal waters and coastal lagoons showing a positive correlation of AAP numbers and day length (Lamy et al. 2011a; Ferrera et al. 2014). Clearly, the environmental data signalize that light has a profound influence in the long term. The light-derived energy increases the bacterial growth efficiency of AAP species. Also, it has been documented that light enhances survival of AAP bacteria under nutrient starvation (Shiba 1984; Soora and Cypionka 2013). Both the effects become apparent only in the long term, but represent a strong competitive advantage and increase fitness of AAP bacteria over heterotrophic species. Among other environmental factors influencing AAP abundance seems to be temperature. The positive effect of temperature was observed in all seasonal studies from both coastal waters (Mašı́n et al. 2006; Zhang and Jiao 2007; Lamy et al. Koblı́žek 863 AAP abundance [103 cells mL-1 ] 0 10 20 30 40 50 0 20 Depth [m] 40 60 80 100 AAP abundance Chlorophyll a Temperature 120 140 0.0 0.1 0.2 0.3 0.4 0.5 Chlorophyll concentration [mg m-3 ] 10 15 20 25 30 Temperature [ºC] Figure 7. Depth profiles of AAP abundance, chlorophyll a concentration and temperature in the Balearic Sea, station ‘D’, September 2007 (Hojerová et al. 2011). 8 6 150 4 100 2 50 0 0 Mar May Jul Sep Nov Jan Mar May Jul Sep 25 20 15 10 Temperature [ºC] AAP biomass Chlorophyll Temperature Chlorophyll a [mg m -3 ] AAP biomass [mg Cm -3 ] 200 5 0 Nov 2004 - 2005 Figure 8. Seasonal changes in microbial community in Čertovo Lake during 2004–05. The abundance of AAPs was determined by IR epifluorescence microscopy as the surface area of BChl a positive cells (Mašı́n et al. 2008). 2011a; Ferrera et al. 2014) and freshwater lakes (Mašı́n et al. 2008; Čuperová et al. 2013; see Fig. 8). However, the correlations of AAP abundance and temperature are relatively weak and overlapping with other factors. Interestingly, a seasonal study from the East China Sea documented higher AAP percentages during the winter period, despite the fact that the total AAP abundance was higher in summer (Zhang and Jiao 2007). Till now, it is not clear whether temperature itself stimulates the growth of AAP bacteria or if the effect is only indirect. In many inland lakes and some marine environments, the water temperature reflects the integrated sum of received solar radiation during the season (Ferrera et al. 2014). As such the observed correlations may simply reflect the long-term positive effect of light on both photoheterotrophic organisms and on autochtonous production of organic carbon by phytoplankton. An intensively discussed issue represents a specific relationship between AAP species and phytoplankton. AAP bacteria are frequently present in algal cultures (Prof. Michael Sieracki, pers. comm.). Several AAP strains were isolated from cultures of the dinoflagellates Alexandrium ostenfeldii and Prorocentrum lima 864 FEMS Microbiology Reviews, 2015, Vol. 39, No. 6 (Allgaier et al. 2003). Four of the obtained isolates were later formally described as Dinoroseobacter shibae, Roseovarius mucosus, Hoeflea phototrophica and Labrenzia alexandrii (Biebl et al. 2005a,b; Biebl, Tindall and Wagner-Döbler 2006; Biebl et al. 2007). The exact mode of coexistence of AAP bacteria and algae is not clear. Both species may live freely in the absence of their partner, but it seems that there is a mutual benefit living in coculture. One of the possible explanations is that algae provide organic carbon for AAP bacteria in exchange for vitamins, and that the algae are not able to produce themselves. This hypothesis seem to be confirmed by the experiments where D. shibae stimulated the growth of the dinoflagellate P. minimum, probably by providing vitamins B1 and B12 (Wagner-Döbler et al. 2010). Surprisingly, at later stages of the cocultivation experiments this mutualistic relationship broke and the bacterium killed its algal host (Wang et al. 2014). While laboratory data on the relationship of AAP bacteria and algae are accumulating, the information from the field is very limited. A study investigating the influence of algal blooms on AAP communities in the East China Sea documented that AAP abundance was frequently higher at stations with diatom or dinoflagelate blooms (Chen, Zhang and Jiao 2011). An exception was the bloom of dinoflagellate Akashiwo sanguinea where the AAP numbers were low (Chen, Zhang and Jiao 2011). The results indicate that the association between AAP bacteria and algae is likely to be complex and species specific. Clearly, the phenomenon deserves more attention. An important ecological issue is whether AAP bacteria are planktonic free-living organisms or mostly particle-attached organisms. Interestingly, most of the first cultured AAP species originated from seaweeds, algal mats or stromatolites (Shiba, Simidu and Taga 1979b; Yurkov and Gorlenko 1990; Nishimura et al. 1994). AAP species were detected in epilithic river biofilms (Hirose et al. 2012) and plant surfaces (Atamna-Ismaeel et al. 2012). Many cultured AAP species also form aggregates and adhere to the culture vessels. The situation in the field is a matter of dispute. Kolber et al. (2000) reported that most of the AAP bacteria in the subtropical Pacific pass through the GF/F filter, which suggests that the community is composed mostly of free-living single cells smaller than 0.7 μm. A very different picture was found in Chesapeake and Delaware estuaries where 30–94% of total AAP bacteria were particle attached (Waidner and Kirchman 2007; Cottrell, Ras and Kirchman 2010). A larger survey conducted by Lami et al. (2009) documented that the proportion of free-living and particle-attached AAP bacteria varied among the environments. In off-shore and open ocean environments, the majority of the AAP communities were small (<0.8 μm) freeliving cells whereas in coastal regions up to one third of the AAP community was particle attached. A large fraction of particleattached AAP cells was also observed in freshwater lakes (Mašı́n et al. 2012). It seems that AAP bacteria do not exhibit any enhanced tendency to attach to particles when compared to heterotroph species. On the other hand, metabolically active AAP bacteria may benefit from the nutrient-rich microenvironment in the particles. The particle-attached lifestyle may also provide protection against grazing. THE ROLE OF AAP BACTERIA IN THE MICROBIAL LOOP The microbial activity of AAP bacteria and their role in biogeochemical cycles remains an open question. Since the AAP bacteria lack carbon fixation capacity and depend on organic carbon substrates, they have to be regarded as secondary producers due to their role in recycling DOM. On the other hand, the capacity of utilizing light energy may help these organisms to better utilize available resources. Laboratory experiments documented that AAP bacteria have significantly higher bacterial growth efficiency when grown in a light–dark regime, i.e. they accumulate more biomass per unit of supplied substrates (Biebl and Wagner-Döbler 2006; Hauruseu and Koblı́žek 2012). This gives AAP bacteria (when grown in light) a clear competitive advantage over chemoheterotrophs with lower growth efficiencies. One can speculate that additional energy obtained from light may even help AAP bacteria to utilize some low energetic or recalcitrant carbon sources. However, the direct proof of such capacity is so far missing. Despite all the uncertainties, AAP bacteria appear to be a highly active part of the microbial community. Experiments conducted in the Delaware estuary documented that AAP cells incorporated approximately two times more 3 H-leucine when compared to average bacteria (Stegman, Cottrell and Kirchman 2014). Similarly, it was shown that AAP bacteria have approximately three times higher frequency of dividing cells when compared to heterotrophic bacteria (Liu, Zhang and Jiao 2010). High activity of AAP bacteria also signalized high levels of puf and bch genes registered in the metatranscriptome of the microbial community collected at the ALOHA station in the Pacific Ocean (Frias-Lopez et al. 2008), despite the fact that AAP bacteria are not very abundant in these oligotrophic waters (Cottrell, Mannino and Kirchman 2006; Ritchie and Johnson 2012). A question arises why there are so few AAP bacteria given that they are so metabolically active? Why do they not dominate the bacterial communities in the euphotic zones? The answer is more complex. Firstly, the euphotic zones of the oceans actually seem dominated by photoheterotrophic species. Over the last 15 years, it has become established that large numbers of bacteria within the euphotic zone contain proteorhodopsin molecules which seem to serve for light harvesting (Béjà et al. 2000; Eiler 2006; Béjà and Suzuki 2008). Moreover, Prochlorococcus, the dominant phytoplankton species in the oligotrophic ocean, may also employ photoheterotrophic assimilation of various organic carbon sources (Zubkov 2009). Thus, photoheterotrophy and mixotrophy seems to be widespread in many aquatic environments and AAP bacteria are just one of many photoheterotrophic groups using this strategy. Secondly, the ability to use light energy helps AAP bacteria to better utilize the available substrate. This provides a competitive advantage mainly under carbon-limited conditions. However, the microbial growth is, in most of the upper ocean environments, limited by the availability of other nutrients: nitrogen, phosphorus and in some areas also iron (Church 2008). Under such conditions, AAP bacteria do not seem to have any strong advantage above regular chemoheterotrophic species. On the contrary, their larger cell sizes restrict the diffusion of nutrients, and their larger genomes, requiring more phosphorus, may (under phosphorus starvation) actually represent a disadvantage. Lastly, the abundance of AAP bacteria may be significantly reduced by grazing. Microscopic analyses of open ocean (Sieracki et al. 2006) and estuary (Kirchman et al. 2014; Stegman, Cottrell and Kirchman 2014) bacterial communities documented that AAP bacteria were on average larger than regular heterotrophic bacteria. The larger size likely makes AAP bacteria more vulnerable targets for protist grazing. It has been suggested that BChl a can be used as a natural in situ tracer, as its decay during the day reflects AAP mortality (Koblı́žek et al. 2005). Using this approach, it has been found that in the Atlantic oligotrophic gyres BChl a Koblı́žek 865 4 BChl a turnover [days -1 ] Villefranche Bay 3 North Atlantic 2 Equatorial Atlantic W Mediterranean 1 Sargasso Sea 0 0.0 0.1 0.2 0.3 0.4 0.5 0.6 -3 Chlorophyll a [mg m ] Figure 9. Relationship between bacteriochlorophyll a turnover and chlorophyll concentration. Each datapoint represents an average value from two to five individual diel measurements. The Atlantic Ocean and Villefranche Bay data were taken from Koblı́žek et al. (2007). Western Mediterranean data from Hojerová et al. (2011). decayed at rate of 0.7 d−1 which should be proportional to AAP mortality. Under stable steady-state conditions, the high mortality rates have to be balanced by equally rapid growth rates. This signalizes that AAP bacteria in oligotrophic regions divide at a rate of one division per day. In more productive marine regions, such as the Equatorial upwelling and North Atlantic, AAP bacteria decayed at rates of two to three divisions per day (Koblı́žek et al. 2007). A similar situation was also observed in the coastal regions of the Mediterranean Sea (Hojerová et al. 2011, see Fig. 9). The higher growth rates of AAP bacteria were also confirmed during manipulation experiments conducted in coastal Mediterranean waters. In treatments where grazing pressure was reduced by filtration or dilution, the proportion of AAP bacteria increased rapidly, reaching up to 20% of total bacteria (Ferrera et al. 2011), documenting that the relatively low numbers of these organisms in nature are caused by a strong grazing pressure. The calculated AAP growth rates were about two times higher than those determined for average bacteria (Ferrera et al. 2011). The available data document an important contribution of AAP to the carbon cycle. AAP bacteria represent 1–7% of total bacteria in the euphotic zones of the oceans (see Table 1), but their cells are on average two times larger than average bacteria (Sieracki et al. 2006). Moreover, in some environments AAP bacteria exhibit faster growth rates when compared to other bacteria (Ferrera et al. 2011). As a result, the contribution of AAP bacteria to the total bacterial (secondary) production may be significantly higher than their abundance alone would indicate. All the presented data indicate that AAP bacteria are metabolically active rapidly growing species with many enzymatic activities (in spite of the fact that even among AAP bacteria there may exist significant heterogeneity with more or less active species). The increasing number of genomic sequences (see Table S3, Supporting Information) document that AAP species possess relatively large genomes, 3.1–4.8 Mb for Roseobacter-related AAP species, 3.6 Mb for gammaproteobacterium HTCC2080 and 4.3 Mb for Congregibacter litoralis (Fuchs et al. 2007), 3.3 Mb for Erythrobacter sp. NAP1 (Koblı́žek et al. 2011), 3.41 and 3.03 Mb for phototrophic Limnohabitans species (Zeng et al. 2012), encoding a large variety of enzymatic functions. In contrast, the genome of Pelagibacter ubique, a cultivated member of the ubiquitous SAR11 clade containing the proteorhodopsin gene, is only 1.3 Mb (Giovannoni et al. 2005). Interestingly, the bacterial groups like Roseobacter clade, gammaproteobacterial clade NOR5/OM6 or Limnohabitans, which are known to harbor AAP species, are all very metabolically active and conduct a more generalist life strategy. The larger genome sizes in these species come from their large enzyme inventory in general, and not from photosynthesis genes. Actually, the cell machinery for anoxygenic phototrophy is only encoded by 30–40 genes and represents about 1% of the total genome (Swingley et al. 2009; Yurkov and Hughes 2013; Zheng et al. 2013). From this perspective, the ability to use light appears as only one of many alternative enzymatic functions in the metabolic portfolio of these versatile organisms. CONCLUDING REMARKS Since the discovery of AAP bacteria by Harashima and Shiba in 1970s, these organisms have become commonly known among aquatic microbiologists studying both marine and limnic environments. Interestingly, it seems that AAP bacteria are not restricted to only aquatic environments as they are being found in many unexpected habitats such as soil crusts (Csotonyi et al. 2010), phyllospheres (Atamna-Ismaeel et al. 2012; Stiefel, Zambelli and Vorholt 2013), biofilms (Hirose et al. 2012) or Antarctic Sea Ice (Koh, Phua and Ryan 2011). The effort of many researchers clarified most of the basic questions regarding their physiology, diversity and distribution. The initial exploratory phase of AAP research is almost over. To further expand our understanding of this interesting group, it is necessary to apply new approaches and ask novel questions. One of the crucial questions remains how and to what extend AAP bacteria actually benefit from light under natural (field) conditions. It is clear that the capacity to generate energy through anoxygenic photosynthesis is beneficial in many different habitats. Many questions however remain. Do we find AAP bacteria 866 FEMS Microbiology Reviews, 2015, Vol. 39, No. 6 in permanently dark habitats such as the deep ocean? Does light only provide ATP for the cell maintenance and metabolism or does the anoxygenic photosynthesis makes it possible to utilize substrates and nutrients which would otherwise not be accessible? Does light help AAP bacteria to use recalcitrant organic carbon? Does light energy stimulate phosphorus or nitrogen acquisition? To answer these questions, it is necessary to conduct carefully designed experiments in the field. The impact of experimental treatments has to be studied using all available tools, such as epifluorescence microscopy and pigment analyses. The community structure can be analyzed using next generation sequencing tools. There are still some novel AAP species to be isolated. Cultivation on agar plates has proven to be a suitable strategy for the isolation of novel species, but novel approaches such as serial dilutions (Salka et al. 2008), micromanipulation (Stiefel, Zambelli and Vorholt 2013) or fluorescence-activated cell sorting in combination with appropriate optical screening may allow the isolation of species which defy growth on solid media. The high diversity of AAP bacteria and their obvious relationship to purple non-sulfur bacteria raises the question of their phylogenetic origin. The current explosion of genome sequencing data may help to explore these questions and put to test various evolutionary scenarios. It seems that the evolution of phototrophy in Proteobacteria is a very complex phenomenon (Nagashima et al. 1997; Koblı́žek et al. 2013) and has to be explored step by step divided in better managable pieces (Boldareva-Nuianzina et al. 2013; Koblı́žek et al. 2015). Another field which still has to be explored is AAP physiology. Under which conditions do AAP bacteria express their phototrophic apparatus? Many species do not express pigments under laboratory conditions, but they probably use photosynthesis in the field under specific conditions (Voget et al. 2015). This fact has an important implication for the role of these organisms in the geochemical cycles, since it signalizes that, in the natural environment they can act as either heterotrophic or photoheterotrophic organisms depending on the actual environmental or physiological conditions. In Roseateles depolymerans, it has been suggested that bacteriochlorophyll expression is expressed under low carbon conditions (Suyama et al. 2002). A similar phenomenon was also observed in Hoeflea phototrophica (Biebl and Wagner-Döbler 2006), but more details are so far missing. Careful laboratory experiments with cultured species with known genomes will allow us to study changes in total gene expresion (Tomasch et al. 2011) and the influence of various environmental stimuli (light, oxygen concentration, nutrient status). When integrated with protein and metabolic profiles, these modern techniques will provide a once unthinkable wealth of data which will help to understand the physiology and metabolism in all its complexity. In summary, all the available data show that AAP bacteria are common in many aquatic environments. They are metabolically active organisms, rapidly utilizing a variety of potential substrates and energy sources, including light. This enables them to maintain higher growth rates when compared to more specialized organisms. In result, large and rapidly growing AAP cells contribute more significantly to the secondary production and aquatic carbon cycling than it would appear from cell numbers alone. SUPPLEMENTARY DATA Supplementary data are available at FEMSRE online. ACKNOWLEDGEMENTS MK thanks Prof. David L. Kirchman, Dr Yonghui Zeng, Dr Isabel Ferrera and the anonymous reviewers for their valuable comments and suggestions on this text. Thanks also to Dr Marcus Tank for providing his pufM sequences from the Baltic Sea lagoon. FUNDING This research was supported by Czech Science Foundation project 13-11281S and project Algatech plus (LO1416). Conflict of interest. None declared. REFERENCES Achenbach LA, Carey J, Madigan MT. Photosynthetic and phylogenetic primers for detection of anoxygenic phototrophs in natural environments. Appl Environ Microb 2001;67:2922–6. Allgaier M, Uphoff H, Felske A, et al. Aerobic anoxygenic photosynthesis in Roseobacter clade bacteria from diverse marine habitats. Appl Environ Microb 2003;69:5051–9. Atamna-Ismaeel N, Finkel O, Glaser F, et al. Bacterial anoxygenic photosynthesis on plant leaf surfaces. Environ Microbiol Rep 2012;4:209–16. 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