Download Biogeography of thermophilic phototrophic

FEMS Microbiology Ecology, 92, 2016, fiw012
doi: 10.1093/femsec/fiw012
Advance Access Publication Date: 28 January 2016
Research Article
RESEARCH ARTICLE
Biogeography of thermophilic phototrophic bacteria
belonging to Roseiflexus genus
Vasil A. Gaisin1,∗ , Denis S. Grouzdev1 , Zorigto B. Namsaraev2,3 ,
Marina V. Sukhacheva1 , Vladimir M. Gorlenko2 and Boris B. Kuznetsov1
1
Institute of Bioengineering, Research Center of Biotechnology of the Russian Academy of Sciences, Leninsky
Ave., 33, bld. 2, Moscow 119071, Russian Federation, 2 Winogradsky Institute of Microbiology, Research Center
of Biotechnology of the Russian Academy of Sciences, Leninsky Ave., 33, bld. 2, Moscow 119071, Russian
Federation and 3 Department of Biotechnology and Bioenergy, National Research Centre ‘Kurchatov Institute’,
Akademika Kurchatova pl., 1, Moscow 123182, Russian Federation
∗
Corresponding author: Institute of Bioengineering, Research Center of Biotechnology of the Russian Academy of Sciences. Leninsky Ave., 33, bld. 2,
Moscow 119071, Russian Federation. Tel: +7(499)135-12-40; E-mail: [email protected]
One sentence summary: The analysis of 16S rRNA gene sequences and environmental data revealed the existence of the specific phylogeographic
pattern for thermophilic phototrophic bacteria belonging to Roseiflexus genus.
Editor: Riks Laanbroek
ABSTRACT
Isolated environments such as hot springs are particularly interesting for studying the microbial biogeography. These
environments create an ‘island effect’ leading to genetic divergence. We studied the phylogeographic pattern of
thermophilic anoxygenic phototrophic bacteria, belonging to the Roseiflexus genus. The main characteristic of the observed
pattern was geographic and geochronologic fidelity to the hot springs within Circum-Pacific and Alpine-HimalayanIndonesian orogenic belts. Mantel test revealed a correlation between genetic divergence and geographic distance among
the phylotypes. Cluster analysis revealed a regional differentiation of the global phylogenetic pattern. The phylogeographic
pattern is in correlation with geochronologic events during the break up of Pangaea that led to the modern configuration of
continents. To our knowledge this is the first geochronological scenario of intercontinental prokaryotic taxon divergence.
The existence of the modern phylogeographic pattern contradicts with the existence of the ancient evolutionary history of
the Roseiflexus group proposed on the basis of its deep-branching phylogenetic position. These facts indicate that
evolutionary rates in Roseiflexus varied over a wide range.
Keywords: microbial biogeography; phylogeography; geotype; bacterial speciation; evolutionary rates; Roseiflexus
INTRODUCTION
The studies of the last 15 years show that microbial distribution is determined not only by environmental factors but also
geographical/historical ones (Martiny et al. 2006; Hanson et al.
2012; Lindström and Langenheder 2012). This modern view was
summarized by van der Gast: ‘Some things are everywhere and
some things are not. Sometimes the environment selects and
sometimes it doesn’t’ (van der Gast 2015). Here, the author transformed the Baas-Becking hypothesis: ‘Everything is everywhere,
but, the environment selects’ (Baas-Becking 1934) which postulated the exclusive ecological approach in study of microbial diversity and distribution.
Data that clearly prove the significance of historical factors were obtained while studying the population structure of
Received: 26 October 2015; Accepted: 27 January 2016
C FEMS 2016. All rights reserved. For permissions, please e-mail: [email protected]
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FEMS Microbiology Ecology, 2016, Vol. 92, No. 3
hyperthermophilic archaea belonging to the genera Sulfolobus
(Whitaker, Grogan and Taylor 2003) and Pyrococcus (EscobarPáramo, Ghosh and DiRuggiero 2005), as well as after a study
of biogeography of thermophilic cyanobacteria belonging to
the genera Synechoccocus (Papke et al. 2003) and Mastigocladus
(Miller, Castenholz and Pedersen 2007). In all the mentioned
cases, specific conditions of hydrothermal springs were responsible for the phenomenon called ‘island effect’ (Hreggvidsson et al. 2012). However, such effect was not revealed
for mesophilic cyanobacteria (van Gremberghe et al. 2011); in
this case, the higher resolution power of genetic markers is
required.
Apparently, stenobiont microorganisms, including thermophiles, are affected by the process which is similar to vicariance for animals. The organisms with more restricted ecologic abilities are known to be more endemic (Barberán et al.
2014). Thus, the modern phylogenetic patterns of thermophilic
prokaryotes should reflect the historical factors influencing the
distribution of genetic lineages.
The objects of the current study were bacteriochlorophyll-a
containing filamentous thermophilic bacteria, belonging to the
Chloroflexi class. These bacteria inhabit thermophilic cyanobacterial mats and in some cases form very thick red-colored layers
(Boomer et al. 2000, 2002). Isolated pure cultures of the representatives of this group were described as filamentous anoxygenic
phototrophic bacteria (FAPB) of the Roseiflexus genus. At the moment, three pure cultures are available in microbial collections:
Roseiflexus castenholzii isolated from Nakabusa hot spring, Japan
(Hanada et al. 2002), Roseiflexus sp. RS-1 and RS-2 isolated from
Octopus hot spring, Yellowstone, North America (van der Meer
et al. 2010). These bacteria are obligate thermophiles growing at
45–60◦ C (Topt. = 50◦ C for R. castenholzii and 55–60◦ C for Roseiflexus
sp. RS-1 and RS-2).
The presence of Roseiflexus-like phylotypes has been revealed in microbial communities inhabiting hydrotherms of
Japan (Hanada et al. 2002; Everroad et al. 2012), Yellowstone
(Boomer et al. 2002, 2009; Nübel et al. 2002; Spear et al. 2005), Kamchatka Peninsula (Burgess et al. 2012; Akimov et al. 2013), Thailand (Portillo et al. 2009), Bulgaria (Tomova et al. 2010), Tibet (Lau
and Pointing 2009; Lau, Aitchison and Pointing 2009) and Andes (Engel, Johnson and Porter 2013). Recently, a new Roseiflexuslike phylotype with a 3% variance (difference) from the known
16S rRNA gene, was found in the cyanobacterial mat of Alla hot
spring (Buryat Republic, Russia) (Gaisin et al. 2015). According to
the recently obtained data, the same phylotype is also present in
Tsenher hydrotherm (Mongolia). The presence of FAPB belonging to R. castenholzii phylotype in Thermophilny hot spring (Kamchatka) has also been revealed.
As a result of the statistical and cluster analysis of the
Roseiflexus-like 16S rRNA sequences, along with data on habitats
where the phylotypes were observed, we propose the existence
of a specific phylogeographic pattern for bacteria belonging to
the Roseiflexus genus.
MATERIALS AND METHODS
Original sequences from Tsenher and Thermophilny
hot springs
The Roseiflexus-like sequences from Tsenher (Mongolia, Global
Positioning System (GPS) coordinates: 47.316667, 101.653611)
and Thermophilny (Kamchatka, GPS coordinates: 54.816667,
160.016667) hot springs were presented for the first time in this
study. Sequences from the Tsenher hot spring were obtained by
analyzing the cloned 16S rRNA gene polymerase chain reaction
(PCR) fragments, amplified from the total DNA of the cyanobacterial mat with primers Univ27F/Univ1492R (Lane 1991).
Sequence from the Thermophilny hot spring was obtained
using Roseiflexus-specific 16S rRNA primers Rof97f/Rof940r. The
detailed procedures of DNA extraction and PCR protocols used
were described previously (Gaisin et al. 2015). The temperature
and pH of the sampling site were 62.2◦ C and 8.4, respectively for
the Tsenher hot spring, and 54.0◦ C and 5.9 for the Thermophilny
hot spring.
The clone sequences from the Tsenher hot spring were
deposited in GenBank under accession numbers KT258753–
KT258772. The sequence from the Thermophilny hot spring derived by the Roseiflexus-specific primers was deposited in GenBank under accession numbers KT266780.
Sequence analysis
Roseiflexus-like sequences were retrieved from GenBank using
Basic Local Alignment Search Tool on-line service (http://www.
ncbi.nlm.nih.gov/blast). Phylogenetic reconstructions were performed using MEGA 5.0 (Research Center of Biotechnology of
the Russian Academy of Sciences, Moscow, Russian Federation) (Tamura et al. 2011). Non-metric multidimensional scaling
(nMDS) was performed in R using the statistical packages vegan
(Oksanen et al. 2007) and ecodist (Goslee and Urban 2007). The
three dimensional (3D) plots of nMDS analysis were created with
R package rgl (Adler and Murdoch 2012).
Statistical analyses
Mantel test was used to estimate the correlations between matrices of temperature, water pH, geographic positions of isolation points and genetic distances with a significance testing
against 1000 permutations. Mantel test was performed with R
using the statistical package ecodist (Goslee and Urban 2007).
Vincenty’s formula and GPS coordinates were used to calculate
the geographic distances between isolation points.
RESULTS
Sets of Roseiflexus-like sequences of 16S rRNA gene
Sequences with a similarity level higher than 95% to R. castenholzii (CP000804) and Roseiflexus RS-1 (CP000686) were retrieved
from GenBank. According to (Tindall et al. 2010), the selected
sequences belonged to the representatives of the same genus.
The sequences found in GenBank together with the sequences
obtained during this study were assembled into the primary
dataset of Roseiflexus-like sequences (Table S1, Supporting Information). The majority of the sequences originated from the
Yellowstone hot springs (Fig. S1, Supporting Information). For
further analysis, the region between the 400th and 1000th nucleotide of the gene was chosen (Fig. S2, Supporting Information)
due to its presence in a maximal number of sequences from all
habitats where the sequences were found. Thereafter, the following sequences were excluded from the primary set: (i) short
sequences not overlapping the above gene region; (ii) sequences
from non-thermophilic and unknown locations; (iii) sequences
with nucleotide anomalies and unambiguous letters. The final
set included 184 sequences (Table S2, Supporting Information),
which originated from 26 thermal springs, 11 of which were located in Yellowstone. Also, the final set represented 12 areas of
hydrothermal activity.
Gaisin et al.
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sequences. Considering the comparison of the geographic map
and the phylogenetic tree, the phylogeography pattern was observed on the global scale (Fig. 2). The result of phylogenetic
reconstruction based on phylogenetic dichotomy clustering is
similar to the nMDS scheme. The main feature of the resulted
phylogenetic tree is that every separate cluster on it included
sequences retrieved from a single restricted geographic region.
The exception is the fact that sequences obtained from Yellowstone hot springs belonged to two separate distant clusters. One
of these clusters included sequences found in hydrotherms of
North and South Americas, whereas the second one consisted
of sequences found in Eurasia.
All Roseiflexus-like sequences were detected in hot springs
from regions whose hydrothermal activity is determined by
the geological dynamics in the Circum-Pacific and AlpineHimalayan-Indonesian orogenic belts (Collins et al. 2011).
Effect of geographic distance on phylogenetic
divergence
Figure 1. nMDS-derived clusters of Roseiflexus-like sequences. The color of the
spheres corresponds to the color of the regional names.
Cluster analysis of Roseiflexus-like sequences
nMDS was used to analyze the sequence clustering. The results were performed in 3D graphic reconstruction (Fig. S3, Supporting Information). The most informative projection of 3D reconstruction is as shown in Fig. 1. According to the obtained
data, Roseiflexus-like sequences formed groups corresponding
to the geographic regions from where these sequences were
obtained. The sequences from various sources formed separate non-overlapping groups while sequences from Yellowstone
springs formed two separate groups.
Maximum Likelihood algorithm was used to construct
the dendrogram of phylogenetic similarity of 16S rRNA gene
Mantel test was used to analyze correlations between genetic
and geographic distances, as well as water temperature and
pH. The results obtained supported non-random correlation between parameters of genetic and geographic distances with a
high probability (Fig. 3), R2 = 0.3446, P < 0.0001. No effect was
found for pH and water temperature on clustering; R2 = 0.0026,
P = 0.3098 for pH and R2 = 0.0012, P = 0.4926 for water temperature correspondingly (Fig. 3).
DISCUSSION
The results obtained during our study are in agreement with the
‘Geotype-plus-Boeing’ model proposed by Cohan and Perry (Cohan and Perry 2007). According to the model, the whole group of
Roseiflexus bacteria is considered to be a uniform ecotype, that is
‘group of bacteria that are ecologically similar to one another, so
Figure 2. Global distribution of Roseiflexus-like sequences. The tree was generated using maximum likelihood method. Bootstrap values were calculated through the
comparison of 1000 alternative trees. DTAM-Digital Tectonic Activity Map (Lowman et al. 1999).
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FEMS Microbiology Ecology, 2016, Vol. 92, No. 3
Figure 3. The results of Mantel test. Relationships between genetic distances and geographic distances (panel a), Relationships between genetic distances and pH
(panel b), Relationships between genetic distances and temperatures (panel c). The values on the axis of temperature, pH and genetic distances are given as Euclid
distances.
similar that genetic diversity within the ecotype is limited by a
cohesive force’ (Cohan and Perry 2007). The main features determining the Roseiflexus-ecotype are obligate thermophily and ecological/physiological dependence from cyanobacteria in mats
that provide a nutrient feeding (van der Meer et al. 2005; Klatt
et al. 2013; Rodionova et al. 2015). The high level of sequence homology found within each phylogenetic cluster supports the hypothesis that natural Roseiflexus populations exist under strong
influence of stabilizing selection and these bacteria are stenobionts (Boomer et al. 2002; Klatt et al. 2013; Gaisin et al. 2015).
It therefore means that the Roseiflexus population within each
hydrothermal region is relatively genetically uniform and does
not undergo significant genetic divergence. However, populations from different geographical locations are phylogenetically
different (Fig. 2). They form the so-called ‘geotypes’ (Cohan and
Perry 2007). Altogether the geotypes form the global phylogeographic pattern of the Roseiflexus ecotype.
One of the main features of the Roseiflexus phylogeographic
pattern is that all known Roseiflexus-like sequences were retrieved from habitats situated within the areas of geological activity along subduction zones of the Circum-Pacific and
Alpine-Himalayan-Indonesian orogenic belts (Collins et al. 2011)
(Fig. 2). Microbial communities of Iceland, Middle Atlantic Ridge
and African hydrotherms were studied and to our knowledge
there are no Roseiflexus-like phylotypes (Skirnisdottir et al. 2000;
van der Meer et al. 2008; Tobler and Benning 2011; Tekere et al.
2012; Sahm et al. 2013). Roeselers and co-authors reported about
the 16S rRNA gene sequences from hot spring in Greenland
that were related to Roseiflexus bacteria (Roeselers et al. 2007).
However, additional analysis revealed that these sequences do
not belong to the Roseiflexus ecotype, because identity between
sequences from Greenland and the Roseiflexus bacteria was
93%. Anomalous geographical distribution was also observed for
thermophilic cyanobacteria Synechococcus spp., which was not
observed at all in hot springs in Iceland, Alaska and the Azores,
even though it would eagerly grow in water from Icelandic hot
springs as reported by R.W. Castenholz (Papke et al. 2003).
The observed phylogeographic pattern of the Roseiflexuslike bacteria could be explained by the specific physiological
requirements of these bacteria. Being obligate thermophiles
(Hanada et al. 2002; van der Meer et al. 2010), the Roseiflexus representatives require hydrothermal activity associated mostly with continental rift zones and volcanic activity in plate subduction zones. Moreover, the Roseiflexus does
not produce resting forms (spores, cysts, etc.) and thus can-
not spread over large distances. Hence, we propose that the
Roseiflexus bacteria could migrate from one geothermal area
to another adjacent one along active subduction zones in
the Circum-Pacific and Alpine-Himalayan-Indonesian orogenic
belts. Such scenario is similar to distribution of deep-sea
hydrothermal vent biota along the ocean ridges (Vrijenhoek
2010). However, in our case mechanism of transfer is not
clear.
Most likely, the modern phylogeographic pattern of
Roseiflexus-like geotypes reflects ancient historical legacies,
just like it has already been mentioned by some authors for
extremophilic microorganisms (Takacs-Vesbach et al. 2008;
Bahl et al. 2011). The proposal that Roseiflexus geotypes were
formed under the influence of historical factors is supported by
the region-associated distribution of the Roseiflexus phylotypes
(Fig. 2). The regional correlations were also supported by the
Mantel test results, whereas no correlations were found with
the temperature and pH of spring water (Fig. 3).
The revealed correlation of Roseiflexus-like bacteria habitats
along with the history of the geological activity allows to propose
a timeframe of evolutionary scenario. To our knowledge this is
the first geochronological scenario of intercontinental prokaryotic taxon divergence. According to data on the Earth’s tectonic
evolution and geochronology, the branching order of Roseiflexuslike phylotypes could be the following. About 200 million years
(My) ago (Jurassic), the supercontinent of Pangea started to break
up forming the Atlantic Ocean (Neall and Trewick 2008). Simultaneously, the subduction of ocean floor on the borders of Pangea
started to form the Circum-Pacific orogenic belt and resulted in
an intense volcanic activity (Scotese 1987). After the break up
of Pangaea, the North American plate began drifting westward.
Around 200 My ago, the Pacific coast turned from a passive margin into an active one with multiple signs of hydrothermal activity that is still active today (Sigloch and Mihalynuk 2013). The
formation of South America occurred later, around 110 My ago,
during the opening of the South Atlantic Ocean (Orme 2007). The
scenario of continental plate formation is also modeled in the
PALEOMAP Project (Scotese 2001) (see the beautiful illustration
at http://www.scotese.com/Default.htm). Such order of events
strongly correlates with the branching order of Roseiflexus-like
phylotypes on the corresponding dendrogram; the South American Roseiflexus group is younger than that of North America
(Fig. 2).
The Eurasian cluster is divided into three subclusters: North
Eastern (Kamchatka, Japan and Yellowstone), Central and South
Gaisin et al.
Asian (Buryatia, Mongolia, Tibet, Southern China and Thailand)
and dispersed subcluster which include sequences from Bulgaria and Eastern China.
The formation of the North Eastern subcluster could be
linked to accretion of the intra-oceanic volcanic arcs with Eurasia and North America. These arcs existed in the central part of
the Panthalassa Ocean and were formed in the course of intraoceanic subduction, ∼245–201 My ago (Middle-Upper Triassic)
(Van der Meer et al. 2012). After a northward drift, these volcanic arcs accreted to the continental margins of Western North
America, North-East Asia and Japan ∼145–100 My ago (EarlyMiddle Cretaceous) (Van der Meer et al. 2012).
The Central and South Asian groups could have been formed
during a series of events that followed the India-Eurasia collision. After the break up of Pangaea (200 My ago), the Indian plate
separated from Africa and Antarctica and started moving northward. In ∼65 My ago, India collided with Eurasia (White and Lister 2012). This resulted in the formation of Alpine-HimalayanIndonesian orogenic belt including uplift of the Himalayas and
Tibetan Plateau. The same mechanism may be responsible for
the formation of the Baikal rift zone (Mats and Perepelova 2011).
These events could lead to the increase of hydrothermal activity
along faults formed in the south part of Eurasia (Bulgaria, Tibet,
South China and Thailand) and in the Baikal rift zone (Buryatia
and Mongolia).
It is more difficult to explain the origin of the third group
which includes sequences from Bulgaria and Eastern China.
Taking into account their deep branching, its formation should
have happened a long time ago, while geographical dispersal
could have been caused by a recent transportation (the so-called
Boeing-effect) or other factors (Cohan and Perry 2007). We cannot exclude a possibility of the fact that the neighbor clustering
of Bulgarian and Chinese sequences is an error of the dichotomous Maximum Likelihood analysis. For example, this clustering is not obvious in nMDS analysis (Fig. S3, Supporting Information), but additional data are required.
The results of this study contribute to a problem of the evolutionary rates in deep-branching bacteria that is highly disputed
in previous years (Dvořák et al. 2015; Plata, Henry and Vitkup
2015; Schopf et al. 2015). Thermophilic FAPB are considered to
be one of the most ancient living organisms on Earth (CavalierSmith 2010). According to the modern reconstructions, the average water temperature of Precambrian ocean was about 55–85◦ C
(from about 3.5 to 2 Gyr ago) (Knauth 2005; Robert and Chaussidon 2006). The microbial mats were formed by anoxygenic phototrophic bacteria, developed in the photic zone of the Precambrian ocean (Tice and Lowe 2004). Perhaps, thermophilic FAPB
were one of these ancient bacteria and had found a way to survive up to date in hydrothermal springs. Earlier results show that
Roseiflexus bacteria are one of the most deep-branching phylotypes among modern FAPB (Grouzdev et al. 2015).
Contrary to these results, the observed phylogeographic pattern of the Roseiflexus bacteria was probably formed during relatively recent geological events. The continents reached their
modern configuration in the Miocene (23–5 My ago), after the
break up of Pangaea that started 200 My ago. In this case, we
can suggest that the tempo of evolution in the Roseiflexus genus
varied over the time from slow long-term to rapid diversification. Also, we did not exclude other scenarios while explaining
the observed pattern. An alternative explanation implies a serial convergence of different ancient phylotypes of Roseiflexus
through horizontal gene transfer, followed by the divergence
of a common phylotype into local populations, thereby erasing
the ancient phylogenetic pattern. A similar scenario was sug-
5
gested recently for cyanobacteria (Dvořák et al. 2014). Another
explanation is that the ancient phylogenetic diversity of Roseiflexus was devastated by environmental change, whereas the
modern diversity of Roseiflexus originated from a survived phylotype. The later scenario was proposed for biogeographic distribution of the local populations of Sulfurihydrogenibium bacteria
in the Yellowstone Caldera (Takacs-Vesbach et al. 2008).
SUPPLEMENTARY DATA
Supplementary data are available at FEMSEC online.
ACKNOWLEDGEMENTS
The authors are grateful to researchers from the Laboratory of
Microbiology at the Institute of General and Experimental Biology, Siberian Branch, RAS, Ulan-Ude, for organizing the expedition to the thermal springs of the Barguzin Valley (Alla) and
Tsenher hot spring. They are also grateful to Dr Kovaleva O. from
Winogradsky Institute of Microbiology RAS, who kindly provided
the sample from Thermophilny (Kamchatka). Special thanks to
Kolganova T.V. and Baslerov R.V. from the Molecular Diagnostics
Laboratory, Centre for Bioengineering RAS. The work was carried out using the scientific equipment of Core Research Facility
of Centre Bioengineering RAS.
FUNDING
This work was supported by Russian Foundation for Basic Research, grant numbers 15-04-07655\15; Russian Federation President Grant NS 6150.2014.4 and Program of the Presidium of
the Russian Academy of Sciences ‘The evolution of the organic
world and planetary processes’.
Conflict of interest. None declared.
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