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We acknowledge the following Institutions/Companies for their support:
Fundação para a Ciência e Tecnologia – FCT
Reitoria da Universidade do Porto
Faculdade de Ciências da Universidade do Porto
Instituto de Ciências Biomédicas Abel Salazar da Universidade do Porto
Centro Interdisciplinar de Investigação Marinha e Ambiental – CIIMAR
Sociedade Portuguesa de Microscopia
Câmara Municipal do Porto
Enzifarma - - Diagnóstica e Farmacêutica, S.A.
VWR International- Material de Laboratório, Lda.
Nzytech – genes and enzymes
Sogrape Vinhos
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Organizing Committee:
Olga Maria Lage, FCUP, Univ Porto
Alexandre Lobo da Cunha, ICBAS, Univ Porto
Damien P. Devos, CABD, UPO, Sevilla
Program
Day 1 – Wednesday, 10 th May
9:00 – 9:45
Registration
9:45 – 10:00
Opening Session
10:00 - 10:30
Warming up talk - Damien P. Devos - The Paradigms They
Are a-Changin’: Past, present and future of your favorite bacteria
10:30 – 11:00
Coffee break
11:00 – 12:00
Keynote speaker - Christian Jogler - Planctomycetes after
the paradigm shift: more exciting than ever!
12:00 - 12:30
Lise Øvreås - Disentangling the extant of Planctomycetes
diversity from numerous habitats
12:30 – 14:00
Lunch
14:00 – 15:00
Keynote speaker – Matthias Horn - Chlamydiae in the
environment - changing our perspective on the C in the PVC Superphylum
15:00 – 15:30 Astrid Collingro - Marine chlamydiae are motile - evidence
from single cell genomes
15:30 – 16:00
Sandra Wiegand - Diversity driven cultivation and genome
sequencing of 80 slow growing Planctomycetes reveal their potential for small molecule
production
16:00 – 16:30
Coffee break
16:30- 17:00
Rita Calisto - Anticancer activity in Planctomycetes
17:00 – 17:30
Olga M. Lage - Planctomycetes: links to the environment
18:00
Welcome reception
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Day 2 - Thursday, 11th May
9:30 – 10:30
Gemmata
Keynote speaker – Siv Andersson - Comparative genomics of
10:30 – 11:00 Coffee break
11:00 – 11:20 Timo Kohn - So close, yet so far – Closest related Planctomycetes can
differ substantially in their genome organizations
11:20 – 11:50 Carlos Santana, Elena Rivas and Sean Stettner - Hopanoid versus
sterol synthesis in PVCs
11:50- 12:10 Julia Endresen Storesund - Planctomycetes distribution along chemical
gradient in the meromictic Lake Sælenvannet
12:10 – 12:30 Milton S. da Costa - The Accumulation of Compatible solutes in
Plantomycetes
12:30 – 14:00 Lunch
14:00 – 15:00 Keynote speaker – Clara Belzer - Verrucomicrobia and the Intestinal
Microbiome: The case of Akkermansia muciniphila
15:00 – 15:30 Laura van Niftrik - The energy-conserving prokaryotic organelle of
anammox Planctomycetes
15:30 - 16:00 Michael Y. Galperin - Bacterial Membrane Energetics and Signaling
from the First Cells to Chlamydia and Kuenenia
16:00 – 16:30 Coffee break
16:30 – 18:00 Enzifarma FCM workshop – Alexandre Salvador – Flow Cytometry
applied to bacterial studies
19:30
20:30
Porto City tour
Dinner by the river
Day 3 - Friday, 12th May
9:30 – 10:30
Keynote speaker – Svetlana Dedysh - Planctomycetes in
wetlands: diversity and ‘omics’-based insights into ecological functions
10:30 – 11:00
Coffee break
11:00 – 11:30
Anastasia A. Ivanova - Metatranscriptome-based insight
into hydrolytic potential of peat-inhabiting Planctomycetes
11:30 – 12:00
Irina S. Kulichevskaya - Abundance and diversity of
Planctomycetes in lichen-dominated sub-Arctic ecosystems of northwestern
12:00 – 12:30
Ice Cave, Northern Norway
Eirik Færøy Sæbø - Novel Planctomycetes from Svarthamar
12:30 – 12:45
Closing session
12:45 – 14:00
Lunch
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Keynote lectures
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Comparative Genomics of Gemmata Species
Siv G.E. Andersson, Mayank Mahajan, Benjamin Yee and John Fuerst
Department of Molecular Evolution, Biomedical Center, Science for Life Laboratory, Uppsala
University, Uppsala, Sweden
Many of the pioneering studies on the Planctomycetes have used Gemmata obscuriglobus
as the experimental model organism. These studies have revealed many unique cellular traits,
such as a highly complex intracellular network of membranes, cell division by budding, spatial
separation of transcription from translation and the ability to take up proteins and complex
sugars from the environment. Despite the importance of G. obscuriglobus as a model organism
for studies of compartmentalized cell plans, no closed genome is available for this species. The
9 Mb draft genome which has been used for inferences of the proteome contains more than
900 gaps. The unfinished status of the genome has been problematic for the interpretations of
the results obtained thus far for many reasons. We will present the closed genome of G.
obscuriglobus along with the genomes of two closely related strains as well as the genome of a
recently described species of a related, but novel genus. First, a phylogeny of their internal
relationships will be presented, onto which we have mapped the flux of protein families. The
comparative analyses indicate a gradual expansion in gene content by duplication and
divergence at most of the ancestral nodes within this bacterial clade. We also noted
remarkable differences in the occurrence of mobile elements among these genomes, with a
massive proliferation of transposons in G. obscuriglobus. Our analyses of the evolution of
potentially new gene functions through expansions, losses and rearrangements of protein
domains in the proteomes of these species will be discussed, along with our interpretations of
why such dramatic changes have occurred.
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Verrucomicrobia and the Intestinal Microbiome:
The case of Akkermansia muciniphila
Clara Belzer
Laboratory of Microbiology, Wageningen University, The Netherlands
The intestinal microbiome is considered as an important modulator of host health. The
Verrucomicrobia is one of the most abundant microbial phyla in the human microbiota,
making up on average 1-4% in the colon. To date, Akkermansia spp. is the only representatives
of the Verrucomicrobia colonizing the intestine. Akkermansia spp. have adapted to the
intestinal environment by specializing in the degradation of host mucin, which it may use as a
sole source of carbon and nitrogen. The mucinases encoded in the genome of Akkermansia
spp. are mostly obtained via horizontal gene transfer from Bifidobacterium spp. and
Bacteroides spp.. In vitro work with Akkermansia muciniphila indicated that the organism is
auxotrophic for growth on an amino acid highly abundant in the peptide core of the mucus
protein. On top of this A. muciniphila is adapted to its host through the ability to use oxygen,
diffusing from host epithelial cells, for higher growth yields.
A. muciniphila has a direct effect on the microbial community structure at the mucosal
layer. Mucus degradation and fermentation by A. muciniphila result in the liberation of
oligosaccharides and subsequent production of acetate, which becomes directly available to
microorganisms in the vicinity of the intestinal mucosa. Co-culturing experiments of A.
muciniphila with the non-mucus degrading butyrate-producing microbes; Anaerostipes caccae,
Eubacterium hallii or Faecalibacterium prausnitzii resulted in syntrophic growth and
production of butyrate. The metabolic interactions of A. muciniphila and butyrigens provide
evidence for a colonic butyrate production pathway that is dependent on host produced
glycans and independent of dietary carbohydrates.
Apart from microbial ecology A. muciniphila is described to directly effect host response. A.
muciniphila possesses anti-inflammatory properties, and has been correlated to protection
against inflammation in diseases such as, type 2 diabetes mellitus, and obesity. In fact, A.
muciniphila treatment can reverse fat gain, serum lipopolysaccharide (LPS) levels, gut barrier
function, and insulin resistance in mice. Immune stimulatory capacities of A. muciniphila lay
partially within its extraordinary outer-membrane structure. Single purified outer-membrane
proteins of A. muciniphila stimulate host immune response through TLR2 (mainly IL6, Il8, Il10,
INFg) and increase trans-epithelial resistance of host cells. On top of this our results have
indicated that pasteurized cells and the outer membrane protein Amuc_1100 can be used as
an oral treatment against fat mas gain and insulin resistance in mice.
In conclusion Akkermansia spp. are a extraordinary group within the Verrucomicrobia. They
are the only Verrucomicrobia adapted to the host intestinal environment. Within the mucosa
Akkermansia spp. directly stimulates host response and a beneficial microbial community. In
light of these findings, future work will gain a better mechanistic understanding and hopefully
the actual role of A. muciniphila in health and disease.
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Planctomycetes in wetlands: diversity and ‘omics’-based insights into
ecological functions
Svetlana N. Dedysh
Winogradsky Institute of Microbiology, Research Center of Biotechnology RAS, Moscow, Russia
Wetlands are ecosystems in which the water table is permanently or periodically close to the
soil surface. These water-saturated terrestrial environments, such as boreal Sphagnum-dominated
peat bogs and lichen-dominated tundra peatlands, are abundantly colonized by members of the
phylum Planctomycetes, which inhabit both oxic and anoxic peat layers. Examination of peat
material by fluorescence in situ hybridization commonly reveals numerous (up to 107 cells per gram
of wet peat) cells of planctomycetes, which are arranged in chains or shapeless cell aggregates and
are mostly attached to the particles of non-decomposed organic material. 16S rRNA gene
fragments from the Planctomycetes comprise 5-13% of total 16S rRNA gene reads retrieved using
high-throughput sequencing techniques from peat samples. Most 16S rRNA gene reads
representing this phylum in Sphagnum- derived peat commonly affiliate with the family
Isosphaeraceae. By contrast, assemblages of planctomycetes in lichen-dominated peatlands of
tundra have a high proportion of representatives affiliated with the Phycisphaera-related group
WD2101 (order Tepidisphaerales). Members of the family Gemmataceae are also common in
boreal and tundra wetlands. Although several peat-inhabiting planctomycetes have been obtained
in pure cultures, little is known about their potential functions in the environment. In order to get
insights into the metabolic potential of planctomycetes, we have assessed their activity response to
amendment of native peat with cellulose, xylan, pectin and chitin, which are the major
biopolymers in Sphagnum-derived peat. The analysis of RNA pool via barcoded Illumina sequencing
revealed that some groups within uncultivated planctomycetes positively responded to the
amendment of peat with various polysaccharides, suggesting the presence of hydrolytic capabilities
in these bacteria. In particular, the strongest substrate-induced response was detected on chitin for
Gemmata- and Phycisphaera-like planctomycetes. Given that routine laboratory tests used for
assessing hydrolytic capabilities are complicated by slow growth rates of peat-inhabiting
planctomycetes, the comparative genomic approach was applied to unveil the hidden potential of
these bacteria. The genomes of two recently described planctomycetes, Paludisphaera borealis
PX4T (family Isosphaeraceae) and Fimbriiglobus ruber SP5T (family Gemmataceae), were sequenced
and analyzed. The genomes encode wide repertoires of carbohydrate-active enzymes (CAZymes)
and large numbers of unclassified putative glycoside hydrolases, suggesting that peat-inhabiting
planctomycetes possess extremely high but partly hidden glycolytic potential and have the ability
to utilize a wide range of natural carbohydrates and glycoconjugates. Notably, the CAZyme
repertoire in planctomycetes significantly differs from those in well-studied hydrolytic bacteria. We
were also able to demonstrate the presence of chitinolytic capability in Fimbriiglobus ruber SP5T,
which was suggested by the results of metatranscriptomic study and the genome analysis. This is
the first member of the order Planctomycetales with confirmed chitinolytic capability. In summary,
the results of our studies suggest participation of peat-inhabiting planctomycetes in degradation of
plant-derived polymers, exoskeletons of peat-inhabiting arthropods as well as exopolysaccharides
produced by other bacteria.
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Chlamydiae in the environment - changing our perspective on the C in
the PVC Superphylum
Matthias Horn
Division of Microbial Ecology, Department of Microbiology and Ecosystem Science,
University of Vienna, Austria
The Chlamydiae, originally considered a small group of closely related bacteria infecting
humans and animals, are much more diverse than recognized previously. A picture is beginning
to emerge, in which the Chlamydiae represent the probably most ancient lineage of
intracellular bacteria; they have adapted to the infection of eukaryotic host cells very early
during evolution, likely during interplay with ancient protists. Extant Chlamydiae comprise
both pathogens of humans and ubiquitous symbionts of amoebae. The discovery of
chlamydiae in the environment not only fundamentally changed our perception of chlamydial
diversity; their analysis also provided new perspectives on evolution and biology of this
important group of intracellular microbes. In this talk I will summarize recent findings about
their unique developmental cycle, their cell biology, and molecular evolution.
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Planctomycetes after the paradigm shift: more exciting than ever!
Christian Jogler
Faculty of Science, Radboud University Nijmegen, The Netherlands
Since their discovery in 1924, Planctomycetes seemed to bluer the pro- / eukaryotic
dichotomy. Their unusual FtsZ-less cell division -mostly through polar budding- their lack of
peptidoglycan and their complex subcellular membrane systems clearly set them apart from all
other bacteria. Ultimately, even a nucleus-like structure with nuclear pores and separation of
transcription and translation was suggested. With the postulation of endocytosis-like uptake of
macromolecules the major eukaryotic hallmark trait required for gaining an endosymbiont was
described for Planctomycetes. Even membrane-coat-like proteins -as in eukaryotes- seemed to
be required for vesicle formation to facilitate endocytosis. With good reason, Planctomycetes
were envisioned as potential ancestors of both, bacteria and eukaryotes and their traits
appeared indeed beyond the bacterium.
However, with the advent of genetic tools, advanced genome research methods and high
resolution imaging systems for light- (dSTORM and SRSIM) and electron microscopy (FIB-SEM
and CET), multiple laboratories provided strong arguments for the Gram-negative cell
architecture of Planctomycetes. Employing such methods, my group recently demonstrated
that Planctomycetes in general lack additional membrane surrounded compartments, but that
their cytoplasmic membrane can create invaginations to store complex carbon substrates in
the enlarged periplasmic space. We further found that at least the suspected MC protein is not
required for macro-molecule uptake and that a process different from endocytosis is
employed to incorporate such molecules. Thus, we reject the hypothesis of the planctomycetal
ancestral relationship with eukaryotes and suggest seeing Planctomycetes as maverick Gramnegative bacteria instead. However, in the past the clear majority of high impact publications
on Planctomycetes focused on such eukaryote-like traits and their potential involvement in
eukaryogenesis. Thus, the findings of others and us will cause a major paradigm shift in the
field of planctomycetal research. One might even ask if Planctomycetes are important to study
after all?
In my talk, I will present further evidence supporting this paradigm shift. I will focus on
what is left of all these planctomycetal curiosities and which novel fields of future research
such as the production of antibiotics or the planctomycetal role in global carbon cycles just
emerged. In the light of these recent findings -without any doubt- Planctomycetes are even
more exciting than ever!
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Oral presentations
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Anticancer activity in Planctomycetes
Rita Calisto1, Eirik Færøy Sæbø2, Lise Øvreås2, Olga M. Lage1,3 and Lars Herfindal4
1
Department of Biology, Faculty of Sciences, University of Porto, Portugal
2
Department of Biology, University of Bergen, Norway
3
Interdisciplinary Centre of Marine and Environmental Research, University of Porto, Portugal
4
Centre for Pharmacy, Department of Clinical Science, University of Bergen, Norway
Planctomycetes has recently been recognized as important candidates for possessing
antibiotic and antifungal activities. They are together with Actinobacteria and Myxobacteria,
known for their bioactive potential and specific characteristics such as large genomes and
complex life cycles. These characteristics make Planctomycetes good candidates for production
of bioactive molecules. Previous in silico genome mining analyses from several Planctomycetes
revealed the presence of genes related to various pathways for the production of several
bioactive molecules, including some antitumor compounds like epothilone. Besides this
potential, no study has up-to-now addressed the anti-cancer proprieties of Planctomycetes. In
fact, this study is the first to approach the planctomycetes’ capacity to induce apoptosis and
decrease cell growth of cancer cell lines.
In this study, twenty-six Planctomycetes strains were screened for their ability to induce
apoptosis and diminish cell growth on an acute myeloid leukaemia cell line and prostatic
cancer cell line. This was achieved by focusing on the solubility of the compounds to see if they
were present on the organic or aqueous phase of the cell extracts. Acute myeloid leukaemia
(AML) and Prostate cancer cell lines were chosen because AML is the one of the most
aggressive forms of leukaemia and, frequently, presents chemoresistance to the treatments,
and prostate cancer is one of the most common cancers and with higher mortality rate,
especially in western countries. Normal rat kidney epithelial cell line (NRK) was used as control.
Assessment of cytotoxic activity was performed by two different methods: first by the
metabolic capacity of the cell culture, using the cell proliferation reagent WST-1, and
thereafter by analysing the percentage of cell presenting apoptotic nuclei, through
microscopy. Our findings indicate that Planctomycetes are producers of anticancer compounds
and of toxins for human cells, with seventeen extracts/strains affecting at least one of the
cancer cell lines, with intermediate or high toxicity. The AML (Molm-13) cells were in general
more sensitive towards the extracts compared to the prostate cancer cells. Moreover, we
identified that the anti-cancer activity induced a delayed cell death, not present in any cell
culture after 24 hours. However, after 72 hours, several extracts had induced cell death in all
cell lines. This screening also demonstrates that the production of compounds is probably
related with the phylogeny of the bacteria, as planctomycetes from the same genera affects
the same type of cells. Strains affiliating to Roseimaritima ulvae, Rhodopirellula lusitana and
Rhodopirellula sp. only affected the AML cell line, while Rhodopirellula baltica affected the
AML cells, the prostatic cancer cells and the control normal cells. Contrarily, Rubinisphaera
brasiliensis did not seem to affect any type of cells. More consistent were the results regarding
the solubility of the produced compounds as all the positive results were obtain from organic
extracts. Finally, the extracts that provoked a higher cell death (over 70% of dead cells) still
affected the cells even after being diluted 4 times. This study provides the first insight on the
effects of the compounds produced by Planctomycetes on human cells, especially cancer cell
lines, demonstrating their amazing potential for biotechnological application.
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Marine chlamydiae are motile - evidence from single cell genomes
Astrid Collingro1, Stephan Köstlbacher1, Mark Mußmann1, Ramunas Stepanauskas2,
Steven J. Hallam3,4, Matthias Horn1
1
Department of Microbial and Ecosystems Science, Division of Microbial Ecology, University of
Vienna, 1090 Vienna, Austria;
2
Bigelow Laboratory for Ocean Sciences, East Boothbay, ME 04544,USA;
3
Department of Microbiology and Immunology, University of British Columbia, Vancouver, BC,
Canada;
4
Genome Science and Technology Program, University of British Columbia, Vancouver, BCV6T
1Z3, Canada
The past two decades revealed an enormous diversity within the chlamydiae. Molecular
data provide evidence for the existence of at least 180 chlamydial families beyond the human
and animal pathogenic Chlamydiaceae. Many of these divergent chlamydiae are of marine
origin and besides limited molecular data no information about their lifestyle and biology is
available so far.
In order to gain insights into the biology of these yet unexplored chlamydiae, and to
understand their genomic diversity and similarity to known chlamydiae, we recovered and
analyzed three chlamydial single-cell amplified genome (SAG) sequences from marine
environments.
Single microbial cells from water samples from the Saanich Inlet (Canada) and the Northern
Sea (Germany), respectively, were sorted by high-speed fluorescence activated cell sorting
(FACS). Genomic DNA of these cells was amplified by multiple displacement amplification
(MDA), and chlamydial SAGs were identified by 16S rRNA gene sequencing. Three chlamydial
SAGs were subsequently sequenced on MiSeq and NextSeq (Illumina) instruments. Sequence
reads were quality checked, assembled with SPAdes, and annotated with ConsPred.
Phylogenetic analyses were performed with MrBayes or RAxML.
Approximately 41-50% of the genome of each SAG could be retrieved, indicating whole
genome sizes of 2.2-2.6 Mbp for these organisms. According to phylogenies of 16S rRNA and
other single copy marker genes, the SAGs represent deeply branching marine chlamydiae.
Their predicted metabolic capabilities are consistent with those reported for other chlamydiae,
including reduced amino acid, vitamin, and cofactor biosynthetic pathways. The presence of
type III secretion genes, ATP/ADPtranslocases, CPAF, Euo and other chlamydia-specific genes
are pointing towards an intracellular lifestyle with the typical biphasic developmental cycle in
these chlamydiae. Surprisingly, all three SAGs harbor genes for chemotaxis and assembly of
flagella. Phylogenetic analysis of flagellar genes suggests a common chlamydial origin of this
trait subsequently lost by all other known chlamydiae.
Analysis of the first SAGs of divergent and so far uncultured marine chlamydiae suggests an
intracellular lifestyle by employing characteristic mechanisms for host interaction known from
other chlamydiae. In addition these chlamydiae have the genetic repertoire for chemotaxis
and motility, which they might use to trace or attach to their hosts. Together this indicates that
albeit the conservation of the genes involved in the basic chlamydial lifestyle, genomes of
divergent lineages bear surprises and are more flexible than previously thought.
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The Accumulation of Compatible solutes in Plantomycetes
Milton S. da Costa,
Centro de Neurociências e Biologia Celular, Universidade de Coimbra, 3001-401 Coimbra,
Portugal.
All microorganisms must adjust, within intrinsic limits, to alterations in the water activity of
the environment. The majority of microorganisms adjust osmotically by the selective
accumulation of small molecular weight organic compounds, such as sugars and sugar
derivatives, polyols, amino acids and amino acid derivatives. Some compatible solutes, namely
trehalose, glutamate and glycine betaine are common compatible solutes of both bacteria and
archaea. Other compatible solutes such as glucosylglycerate and mannosylglyceramide are
very rare and some are restricted to one known organism.
The bacteria of the phylum Planctomycetaeota (Planctomycetes) represent a unique group
of organisms with unique morphologies. Many of these organisms are of marine origin and
should thus accumulate compatible solutes to cope with increases in the salinity of the
environment.
We have examined the compatible solute pools of three planctomycetes to grasp the
diversity of compatible solutes that accumulate in the organisms under salt stress and the
biosynthetic pathways involved in their synthesis.
The species Rhodopirellula baltica accumulates sucrose, glutamate, trehalose and the
extremely rare mannosylglucosylglyerate (MGG) found previously in only two species of
thermophilic Petrotoga of the order Thermotogales). The synthetic pathway of the latter
compatible solute was also determined. The relationship between nitrogen availability and
osmotic adjustment showed that MGG accumulated during growth under low nitrogen levels
in the medium. To extend these results we also examined the biosynthesis and the
accumulation of compatible solutes in two other planctomyces, namely Rubinisphaera
brasiliensis and Gimesia maris. The former accumulated primarily α-glutamate, sucrose,
ectoine and hydroxyectoine. But G. maris also accumulated glucosylglycerate under low
nitrogen levels in the medium. The synthesis and regulation of the accumulation of
glucosylglycerate will be discussed.
14
The Paradigms They Are a-Changin’:
Past, present and future of your favorite bacteria.
Damien P. Devos
Centro Andaluz de Biología del Desarrollo CABD
Universidad Pablo de Olavide-CSIC,
Sevilla, Spain
These are wonderful times for PVC research!
The field is booming, erroneous interpretations have been corrected and we are now facing
a bright future. Let’s hope the funding agencies are listening!
In this talk, I will revisit the past and current efforts in the analyses of the bacterial
Planctomycetes-Verrucomicrobia-Chalmydiae (PVC) superphylum. I will present an historical
perspective on this disparate group of bacteria. I will go back to the early days of PVC research
and follow the evolution of the analyses performed and interpretations presented.
I will then explore the increasing number and diversity of PVC researches observed today. I
will summarize the recent novelties described in the field and how this modified our
perception and interpretations of these bacteria.
Eventually, I will close by presenting a few directions that the PVC field and its happy
community might take in the future.
15
Bacterial Membrane Energetics and Signaling from the First Cells to
Chlamydia and Kuenenia
Michael Y. Galperin
NCBI, NLM, National Institutes of Health, Bethesda, Maryland, USA
The Planctomycetes-Verrucomicrobia-Chlamydiae superphylum is an early-branching
bacterial lineage that could provide valuable clues on the evolution of bacteria. Recent studies
of prokaryotic genome sequences brought about a significant progress in understanding of the
general physiology of bacteria and their metabolic pathways. Components of the membrane
energetics machinery and signal transduction pathways attracted much less attention, owing
largely to the multi-subunit nature of the membrane energy-transducing and signaling
enzymes and their diversity. We have used the Clusters of Orthologous Groups of proteins
(COG) system for a comparative analysis of the PVC bacteria and their ability to utilize protonmotive force and/or sodium-motive force. This study placed the membrane bioenergetics of
PVC members squarely in the bacterial domain but revealed presence of distinct mechanisms
of energy conservation in different lineages, reflecting their likely diversification from the
ancestral sodium-dependent bioenergetics [1-3]. Free-living PVC members often encode both
H+- and Na+-translocating ion pumps and H+- and Na+-translocating ATP synthases. In contrast,
chlamydia show clear signs of loss of membrane enzymes in the course of the adaptation to
the parasitic lifestyle [4,5]. The signaling mechanisms of PVC members also show dramatic
diversity with planctomycetes and verrucomicrobia having some of the most complex signal
transduction machineries among all bacteria, which include two-component signaling,
chemotaxis, Ser/Thr-protein kinases and protein phosphatases, as well as c-di-GMP- and c-diAMP-mediated signal transduction [6,7]. Chlamydia encode greatly streamlined versions of
these systems, which, however, still include two-component, Ser/Thr protein phosphorylation,
and c-di-AMP-mediated signaling. The relatively narrow bioenergetics and signaling
capabilities of chlamydial cells open possibilities for designing potential lineage-specific
antibiotics.
References
1. Mulkidjanian AY et al. (2008) Biol. Direct 3: 13. PMID: 18380897
2: Mulkidjanian AY et al. (2008) Biochim. Biophys. Acta 1777: 985-992. PMID: 18485887
3. Mulkidjanian AY et al. (2012) Proc. Natl. Acad. Sci. USA 109: E821-E830. PMID: 20693418
4. Häse CC et al. (2001) Microbiol. Mol. Biol. Rev. 65: 353-370. PMID: 11528000.
5. Dibrov P et al. (2004) J. Mol. Microbiol. Biotechnol. 8: 1-6. PMID: 15741735.
6. Galperin MY (2005) BMC Microbiol. 5:35. PMID: 15955239.
7. Galperin MY et al. (2010) Mol. BioSystems 6: 721-728. PMID: 20237650.
16
Metatranscriptome-based insight into hydrolytic potential of peatinhabiting Planctomycetes
Anastasia A. Ivanova1, Carl-Eric Wegner3, Werner Liesack2 and Svetlana N. Dedysh1
1
Winogradsky Institute of Microbiology, Research Center of Biotechnology RAS, Moscow,
Russia;
2
Max Planck Institute for Terrestrial Microbiology, Marburg, Germany;
3
Friedrich Schiller University Jena, Institute of Ecology, Aquatic Geomicrobiology, Jena,
Germany
Members of the phylum Planctomycetes are common inhabitants of northern Sphagnumdominated wetlands. The evidence is accumulating that some members of this phylum can be
involved in degradation of organic matter in these ecosystems but the experimental data
remain scarce due to the low number of characterized representatives from this bacterial
group. Here, we aimed to get insights into the metabolic potential of planctomycetes by
monitoring their activity response to amendment of native peat with cellulose, xylan, pectin
and chitin, which are the major biopolymers in Sphagnum-derived peat.
Peat sampled from a Sphagnum peat bog in northern Russia was amended with 500 mg/L of
the polysaccharides mentioned above and incubated for 6 weeks. Insights into community
changes caused by substrate availability were gained by the analysis of rRNA and mRNA pools
via barcoded Illumina sequencing.
A total of 1,638,305 rRNA and mRNA sequences affiliated with the Planctomycetes were
retrieved in our study. The majority (~60%) of 16S rRNA sequences could not be assigned to
taxonomically characterized organisms. Community shifts within the Planctomycetes were
rather distinct depending on the added carbon source. The strongest substrate-induced
response was detected on chitin. The two groups with increased transcript pools were
Gemmata- and Phycisphaera-like planctomycetes. Among uncultivated members of the
Planctomycetaceae, two abundant transcript pools were retrieved from pectin-amended
samples and belonged to Pirellula-like bacteria.
Taken together, metatranscriptome analysis revealed various planctomycetes-like
populations to respond positively to the amendment with polysaccharides, providing evidence
for hydrolytic capabilities in these bacteria.
17
So close, yet so far – Closest related Planctomycetes can differ
substantially in their genome organizations
Timo Kohn1, Sandra. Wiegand1, Patrick Rast2, Manfred Rohde3, Franz Brümmer4, RalfWalter Müller4, Mareike Jogler2 and Christian Jogler1
1
Radboud University, Nijmegen, Netherlands
2
DSMZ, Braunschweig, Germany
3
HZI, Braunschweig, Germany
4
University of Stuttgart, IBBS, Stuttgart, Germany
Since decades, the 16S rRNA gene is the gold standard for the classification of bacteria. But
its resolution, when it comes to close related strains, is restricted. This limitation can be
overcome with the advances in genome sequencing and the comparison of multiple marker
genes or whole genomes as such. Here we show a novel Planctomycete, isolated from a
freshwater sponge, that shows 99% 16S sequence identity with the type strain Planctopirus
limnophila DSM3776T, but differs considerably when the whole genomes are compared. Based
on 16S rRNA sequence identity, this isolate would represent a novel strain, while Average
Nucleotide Identity (ANI) proves that this isolate represents a novel species. Compared to the
type strain, this strain has two different genes encoding for the 16S rRNA and shows
differences in the predicted secondary metabolite gene clusters. Therefore, evaluating the
“novelty” of a strain based on 16S rRNA identity, may leave novel talented producers
undetected.
18
Abundance and diversity of Planctomycetes in lichen-dominated subArctic ecosystems of northwestern Siberia
Irina S. Kulichevskaya, Anastasia I. Ivanova and Svetlana N. Dedysh
Winogradsky Institute of Microbiology, Research Center of Biotechnology of the Russian
Academy of Sciences, Moscow, Russia
Members of the bacterial phylum Planctomycetes inhabit a wide range of aquatic and
terrestrial environments with diverse environmental conditions. Yet, most cultured and
taxonomically characterized representatives of this phylum are mesophiles. At the same time,
planctomycetes are commonly detected in various low-temperature ecosystems by molecular
surveys. This study was initiated in order to assess the abundance and diversity of
planctomycetes in wetlands and upland soils within the zone of forested tundra and
discontinuous permafrost in northwest Siberia with a ground vegetation cover composed of
reindeer lichens (genera Cladonia and Cetraria).
The microbial communities of two lichen-dominated ecosystems typical of the sub-arctic
zone of northwestern Siberia, that is a forested tundra soil and a shallow acidic peatland, were
examined in our study. As revealed by molecular analyses, soil and peat layers just beneath the
lichen cover were abundantly colonized by bacteria from the phylum Planctomycetes. Highest
abundance of planctomycetes detected by fluorescence in situ hybridization was in the range
2.2–2.7 х 107 cells per gram of wet weight. 16S rRNA gene fragments from the Planctomycetes
comprised 8–13% of total 16S rRNA gene reads retrieved using Illumina pair-end sequencing
from the soil and peat samples. Lichen-associated assemblages of planctomycetes displayed
unexpectedly high diversity, with a total of 89,662 reads representing 1723 operational
taxonomic units determined at 97% sequence identity. The soil of forested tundra was
dominated by uncultivated members of the family Planctomycetaceae (53–71% of total
Planctomycetes-like reads), while sequences affiliated with the Phycisphaera-related group
WD2101 (recently assigned to the order Tepidisphaerales) were most abundant in peat (28–
51% of total reads). Representatives of the Isosphaera–Singulisphaera group (14–28% of total
reads) and the lineages defined by the genera Gemmata (1–4%) and Planctopirus–
Rubinisphaera (1–3%) were present in both habitats.
Two isolates of Singulisphaera-like bacteria, strains P12 and P515, were isolated from a
peatland and a forested tundra soil, respectively. The isolates shared identical 16S rRNA gene
sequences, which exhibit only 93–94% sequence similarity to 16S rRNA gene sequences from
members of the genus Singulisphaera and 91–92% sequence similarity to members of the
genus Paludisphaera. Strains P12 and P515 displayed good tolerance of low temperatures (4–
15oC) and were capable of growth on a number of polysaccharides, including lichenan, a
characteristic component of lichen-derived phytomass. Based on the characteristics
determined in our study, we propose to classify the novel planctomycetes as representing a
novel genus and species, ‘Tundrisphaera lichenicola’ gen. nov., sp. nov. Thus, our study
provided the first proof of high planctomycete abundance and diversity in cold, sub-arctic
tundra ecosystems.
19
Planctomycetes: links to the environment
Olga M. Lage1,2, Maria da Conceição Marinho1, Carlos Ramos1, Teresa Carvalho1 and
Sara C. Antunes1,2
1
2
Department of Biology, Faculty of Sciences, University of Porto, Portugal
Interdisciplinary Centre of Marine and Environmental Research, University of Porto, Portugal
Planctomycetes have been found in a broad range of habitats but their precise role in such
environments is not well known. Their physiological capacities make them suitable for sulfated
hydrocarbon degradation playing an important role in mineralization or for the removal of
ammonium and nitrite in the anammox process. The constant accumulation of toxic
compounds such as pharmaceutical drugs can affect the base of the trophic chain, reducing an
important food source to organisms in higher trophic levels. In this work, we explore different
ecological aspects of planctomycetes namely (1) their adequacy to serve as food source for
other organisms in higher trophic levels; (2) their capacity for hydrocarbon degradation; (3) the
impact of pharmaceuticals in their viability. Our studies address thematics still scarcely
explored.
20
Disentangling the extant of Planctomycetes diversity from numerous
habitats
Julia Storesund, Eirik Færøy Sæbø and Lise Øvreås
Department of Biology, University of Bergen, Norway
The phylogenetic positions of 30 isolates that morphologically resemble members of the
family Planctomycetaea were determined by sequencing analyses of the 16S rRNA gene. The
isolates were distributed amongst seven genera, where two represents completely novel
genera. Seven isolates were assigned to the genera Rhodopirellula, 5 to genera Blastopirellula,
7 to the genera Gimesia, 7 to the genera Rubinisphaeara whereas the five last isolates were
found to be only distantly related to previously described Planctomycetes. The collection of
these unique Planctomycetes strains were obtained from different extreme environments,
including deep-sea iron hydroxide deposits (Atlantic Mid Ocean spreading Ridge and the South
Pacific spreading Ridge), 700 years old glacier cave ice, biofilm on kelp from polar waters
around Svalbard, and water masses from a meromictic lake displaying a strong chemical
gradient. Morphological characters and internal membrane structures of the isolates generally
correlates with features described for the order Planctomycetales, but distinct differences
were seen between the isolates. We anticipate that the Planctomycetes are reservoir for
innovative knowledge both regarding the evolution of life and cellular compartmentalisation
processes, which are translated into specialized and novel microbial communities that colonize
various natural environments. The putative role of planctomycetal carbon remineralization is
key for the ecology of many different environments, especially marine sediments and ice
biomes. Given the slow growth of planctomycetes, some species have doubling time up to
several weeks. The high abundance of planctomycetes in certain deep ocean environments
might be driven by the presence of complex carbon sources in contrasting to oligotrophic
surrounding water masses where they are rather scarcely present. Our collection also contains
isolates from the biofilm of kelps where they have to face strong competition and are obliged
to develop scavenging survival strategies like the production of antimicrobials. Functional
analyses of closely related bacteria obtained from widely different environments, could
improve our understanding of such mechanisms, and several of our bacterial strains obtained
from different environments are documented as closely related.
21
Novel Planctomycetes from Svarthamar Ice Cave, Northern Norway
Eirik Færøy Sæbø, Julia Endresen Storesund, Hilde Rief Armo, Stein Erik Lauritzen, Lise
Øvreås
Department of Biology, University of Bergen, Norway
Ice caves are exceedingly conserved and quite unexposed extreme environments,
representing a unique location for studying the impact of darkness, low temperatures and
evolution in time on the organisms living there. The Svarthamar Ice cave in Norway is a two
entrance, dynamic ice cave, possessing the largest Cave room in Scandinavia and is one of the
lowest altitude ice caves in Norway. Radiocarbon dating of plant debris at the base of the ice
mass indicates that the oldest part of the ice is more than 700 years old. So far only few
studies on describing the microbiome of Ice cave have been performed, and to our knowledge
no Planctomycetes isolates have been retrieved from these environments. As the entire
chronosequence is exposed inside the cave we have been able to drill ice samples spanning
this entire time span. The Ice samples were drilled under sterile conditions and the ice cores
were transferred to sterile bottles and transported back to the laboratory in frozen conditions.
The samples were then thawed in the dark and most of the water was collected onto Sterivex
filters for DNA and RNA extractions. DNA and cDNA was amplified using primers targeting the
16S rRNA gene and sequenced using illumina MiSeg approach. 5 ml of the water were used for
two parallel incubations using Planctomycetes specific medium (M30), at 10°C and at room
temperature. Enrichments were carefully monitored by examination in light microscope, and
when cells with characteristics resembling that of Planctomycetes were observed, these were
plated onto solid media (gelrite) for purification. From the descriptive microbial community
analyses 6% of the total reads was found to affiliate to Planctomycetes. From the isolation
procedure, three novel Planctomycetes was found in 2 different samples, two of the isolates
were found in the same sample, incubated at 10°C, and one isolate from the sample incubated
at room temperature. One of the isolates formed colonies that were solid and had a rubberlike consistency, whilst the two other isolates formed colonies with a more creamy
consistency. Light microscopy revealed that two of the isolates shared oval and egg-shaped cell
structure, whilst the other had cells with shapes of a more spherical nature. All isolates
showed clear signs of budding reproduction and formed characteristic rosette structures. The
unique Planctomycete 16S rRNA gene sequences identified in this study were phylogenetically
closely related to sequences from clone sequences from treatment plants in other published
studies. The closest cultivable isolate is Pirellula sp. Schlesner strain 302 isolated from chalk
mine in Germany (90% 16S sequence similarity). This study reveals new insight to diversity of
Planctomycetes and suggests the presence of a novel, cryotolerant genus from glacial
environments.
22
Flow Cytometry applied to bacterial studies
Alexandre Salvador
Enzifarma S.A
Flow Cytometry (FCM) is a powerful technic used to analyze particles in a suspension. The
analyses can go from a simple comparison on the morphological characteristics of the
particles, to their level of autofluorescence. In many cases, the levels of autofluorecence are
not enough to distinguish between particles of interest, and morphology is also difficult
because of the presence of non-biological particles. In these cases, using dyes to stain cells or
cell specific characteristics, cells can be useful to distinguish and correlate parameters. In fact,
Flow Cytometry allows multiparametric measurements. Several parameters can be correlated
at the same time, emphasizing the properties that we want to highlight. Besides identification,
in isolated samples physiological status of the cells can also be addressed. Being able to stain
specific structures or access metabolic status, FCM users can do real-time analyses,
understanding the biological patterns and consequences of stimulus or inhibitors. Due to a
high number of fluorescent probes or molecules that allow to access different cell parameters
or stages, in a real research environment FCM became a powerful simple reliable and rapid
tool. Because of these characteristics bacterial analyses became more popular. The most
common assays involve the capacity to discriminate bacteria from other type of cells, viability
assays and functional assays. The biggest question is always: what test to use, what
fluorochromes? How to combine? What is the correct protocol? The share of experience and
knowledge is highly important and fundamental in this developing area.
23
Hopanoid versus sterol synthesis in PVCs
Carlos Santana1, Elena Rivas-Marin1, Sean Stettner2, E. Gottshall2, M Helling2, F
Basile2, Naomi Ward2 and Damien Devos1
1
Centro Andaluz de Biología del Desarrollo CABD, Universidad Pablo de Olavide-CSIC, Sevilla,
Spain
2
Department of Molecular Biology, Department of Chemistry, University of Wyoming, USA
Membrane composition is central to the multiple roles of membranes in the cell. Hopanoids
and sterols are, respectively, bacterial and eukaryotic polycyclic triterpenoids with important
membrane-ordering function. The two classes of lipids are chemically, structurally, and
functionally related. Few bacterial species have been reported to synthesize sterols, and the
origins and functions of bacterial sterols are unknown. Most Planctomycetes synthesize
hopanoids while Gemmata obscuriglobus is the only PVC member known to synthesize sterols.
Here, we addressed this conundrum using bioinformatics, genetic, and chemical approaches.
Bioinformatics analyses showed that Planctomycetes have undergone an expansion in the
number of hopanoid cyclase genes. In addition, phylogenetic analyses of the sterol synthesis
genes suggested that the assumption of lateral gene transfer for acquisition of these genes by
G. obscuriglobus should be reconsidered. Given the essential nature of eukaryotic sterols, the
logical next step was to investigate the necessity of sterol synthesis for bacterial life, using G.
obscuriglobus as an experimental model. We found that sterols are essential for the growth of
G. obscuriglobus, and that sterol depletion leads to aberrant membrane structures and
budding defects. We also confirmed that chemical inhibition of sterol synthesis leads to dosedependent depletion of membrane sterols, and that both this effect and the related budding
defect could be complemented by provision of exogenous lanosterol (the native G.
obscuriglobus sterol).
To the best of our knowledge, this is the first report of essential sterols in a prokaryotic
species. Our work provides a foundation for pursuit of fundamental questions in evolutionary
cell biology: Why have some bacteria acquired the ability to produce sterols? What are the
advantages of sterols over hopanoids? Why have sterols, and not hopanoids, prevailed in
eukaryotes?
24
Planctomycetes distribution along chemical gradient in the meromictic
Lake Sælenvannet
Julia Endresen Storesund1, Eva-Lena Nordmann1, Hilde Rief Armo1, Anders Lanzèn2
and Lise Øvreås1
1
Department of Biology, University of Bergen, Norway
2
Neiker-Technalia, Spain
Lake Sælenvannet is a meromictic lake located south of Bergen, Norway. The 26 m deep
lake has a small channel, which connects it via the Nordåsvannet to the open sea. The lake is
permanently stratified into two layers. The upper water layer is a brackish layer with major
input from of water runoff from the lake surroundings. The bottom layer consist of old saline
water, with low or no oxygen concentrations. The interface between these two layers is
referred to as “chemocline”. At the chemocline bacteria can have benefits from both layers such as oxygen from the upper layer and reduced sulphur from the bottom layer, and it is
often regarded hot spot for prokaryotic activity. Samples throughout the water column were
collected and microbial community profile analyses were done using 454 high throughput
sequencing in 2012. Planctomycetes related sequences were found both in the oxic and anoxic
parts of the lake, but showed an uneven distribution throughout the water column, with the
highest relative abundances, 10%, in the saline anoxic layer at 15 m depth, 6 % at 5 meters
depth, whereas the surface water and the area around the chemocline had less than 1%
planctomycetes reads. Subsequently, samples for enrichment and isolation of novel
Plantomycetes were collected from seven different depths of the lake in 2014. Ten novel
isolates from four different genera affiliating to the Planctomycetaceae family were obtained
in pure culture. Of these, two strains representing new species within the Rhodopirellula and
Gimesia genera were isolated from the chemocline at seven and nine meters depth
respectively. A second strain obtained from nine meters depth was closely related to
Blastopirellula cremea. Seven isolates retrieved from seven different depths with extensively
different salinities and chemical compositions showed identical 16S rRNA gene sequences, and
likely represent a new species closely associated with the Rubinisphaera genus. The presence
of this novel planctomycete in all water depths spanning the entire chemical gradient could
indicate high phenotypic plasticity in this isolate or a very efficient survival strategy. Overall,
our results indicate the presence of a diverse group of Planctomycetes present in Lake
Sælenvannet, with a strong potential for novel adaptations to chemical stress factors.
25
The energy-conserving prokaryotic organelle of anammox
Planctomycetes
Laura van Niftrik
Microbiology, Institute for Water & Wetland Research, Faculty of Science, Radboud University,
Heyendaalseweg 135, 6525 AJ Nijmegen, The Netherlands
Anammox bacteria perform anaerobic ammonium oxidation with nitrite as electron
acceptor and nitrogen gas as end product. Intermediates of the anammox reaction are nitric
oxide and the “rocket fuel” hydrazine. Anammox bacteria belong to the phylum
Planctomycetes and are recognized as major players in the global nitrogen cycle. It is
estimated that anammox bacteria are responsible for up to 50% of the nitrogen in the air that
we breathe. In addition, anammox bacteria are extremely valuable for wastewater treatment
where they are applied for the cost-effective and environment-friendly removal of nitrogen
compounds. Anammox bacteria harbor a major intracellular compartment called the
anammoxosome (Fig. 1) which is the location of the anammox reaction. Currently we are
investigating how the substrates ammonium and nitrite are transported through the cell to the
anammoxosome and how the anammox reaction is coupled to the anammoxosome
membrane to conserve energy. To this end, we use metagenome, transcriptome and
proteome analysis, subcellular (membrane) fractionation, biochemistry of purified proteins,
activity assays and cryo-transmission electron microscopy. The aim is to unravel the molecular
and biochemical pathway of anaerobic ammonium oxidation.
Fig. 1. Transmission electron micrograph and schematic model of the cell plan of anammox
bacteria. Scale bar: 200 nm.
26
Diversity driven cultivation and genome sequencing of 80 slow growing
Planctomycetes reveal their potential for small molecule production
Sandra Wiegand1, Mareike Jogler2, Anja Heuer2, Patrick Rast2, Anne-Kristin Kaster2,
Olga M. Lage3, Lise Øvreås4, Laura van Niftrik1, John Vollmers2 and Christian Jogler1
1 Microbiology, Institute for Water & Wetland Research, Faculty of Science, Radboud
University, Nijmegen, The Netherlands
2 Microbial Cell Biology and Genetics, Leibniz Institute DSMZ, Braunschweig, Germany
3 University of Porto, Porto, Portugal
4 University of Bergen, Bergen, Norway
Members of the taxon Planctomycetes, that belongs to the PVC superphylum, are
characterized by many unusual features. They show a life style switch during which the sessile
mother cell releases a swimming daughter cell after FtsZ-independent binary fission or polar
budding. Also, planctomycetal genomes encode numerous giant genes and bear the genomic
potential for secondary metabolite production.
As the whole clade is notably under-sampled with relatively few genomic sequences being
publicly available, we focused our efforts on increasing the data basis for comparative studies.
For this purpose, we sampled multiple aquatic habitats around the globe and isolated about 80
new planctomycetal strains from various biotic and abiotic surfaces. Planctomycetes were
enriched by targeting the slow growing antibiotic resistant bacteria in combination with
selective carbon sources. Most of these strains represent novel taxa up to the level of a new
order, capturing an unpreceded degree of diversity. In total, we brought more novel
Planctomycetes into pure culture than currently described species of this phylum exist.
To allow detailed analyses we produced closed as well as high-quality draft genomes of the
novel isolates. The exploration of the gained genomic information not only enables deep
insights into the taxonomy of the phylum and its subtaxa, but also the definition of its core and
pan genome. The latter increases our knowledge on the metabolic versatility and the
environmental role of this phylum. Furthermore, we identified secondary metabolite related
genes and further strengthened our hypothesis of Planctomycetes as talented producers.
27
Participants List
Eduarda Almeida
FCUP, University of Porto, Portugal
[email protected]
Centro Andaluz de Biología del Desarrollo
CABD, Universidad Pablo de Olavide-CSIC,
Spain
[email protected]
Siv Andersson
Department of Cell and Molecular
Biology, Uppsala University, Sweden
[email protected]
Clara Belzer
Laboratory of Microbiology,
Wageningen University, The
Netherlands
[email protected]
Rita Calisto
FCUP, University of Porto, Portugal
[email protected]
Teresa Carvalho
FCUP, University of Porto, Portugal
[email protected]
Laura Claret
Centro Andaluz de Biología del Desarrollo
CABD, Universidad Pablo de Olavide-CSIC,
Spain
[email protected]
Astrid Collingro
Division of Microbial Ecology, Department
of Microbiology and Ecosystem Science,
University of Vienna, Austria
[email protected]
Milton da Costa
Department of Life Sciences, University of
Coimbra
[email protected]
Svetlana Dedysh
Laboratory of Wetland Microbiology,
Winogradsky Institute of Microbiology,
Russia
[email protected]
Damien P. Devos
Teresa Dias
FCUP, University of Porto, Portugal
[email protected]
Michael Galperin
NCBI, NLM, National Institutes of Health,
USA
[email protected]
Ofélia Godinho
Universidade de Aveiro, Portugal
[email protected]
Ana Patrícia Graça
Synthetic Microbiology – Hans Knöll
Institute, Germany
[email protected]
Matthias Horn
Division of Microbial Ecology, Department
of Microbiology and Ecosystem Science,
University of Vienna, Austria
[email protected]
Anastasia Ivanova
Winogradsky Institute of Microbiology,
Research Center of Biotechnology RAS,
Moscow, Russia
[email protected]
Christian Jogler
Faculty of Science, Radboud University
Nijmegen, The Netherlands
[email protected]
Timo Kohn
Faculty of Science, Radboud University
Nijmegen, The Netherlands
[email protected]
Irina Kulichevskaya
Laboratory of Wetland Microbiology,
Winogradsky Institute of Microbiology,
Russia
28
[email protected]
Eirik Færøy Sæbø
Olga Maria Lage
Department of Biology, University of
Bergen, Norway
[email protected]
FCUP, University of Porto, Portugal
[email protected]
Alexandre Lobo da Cunha
ICBAS, University of Porto, Portugal
[email protected]
Conceição Marinho
FCUP, University of Porto, Portugal
[email protected]
Enrique Merino
Universidad Nacional Autonoma de Mexico,
Mexico
[email protected]
Alexandre Salvador
Enzifarma, Portugal
[email protected]
Carlos Santana Molina
Centro Andaluz de Biología del Desarrollo
CABD, Universidad Pablo de Olavide-CSIC,
Spain
[email protected]
José Diogo Santos
FCUP, University of Porto, Portugal
[email protected]
Lise Øvreås
Department of Biology, University of
Bergen, Norway
[email protected]
Claudia Serra
Mónia Pedrosa
Enzifarma, Portugal
[email protected]
Sean Stettner
Departments of Molecular Biology and
Botany, Wyoming INBRE Bioinformatics
Core, USA
[email protected]
Ana Mafalda Pinto
FCUP and CIIMAR, University of Porto,
Portugal
[email protected]
FCUP, University of Porto, Portugal
[email protected]
Carlos Ramos
FCUP, University of Porto, Portugal
Julia Endresen Storesund
Department of Biology, University of
Bergen, Norway
[email protected]
[email protected]
Susana Ribeiro
Enzifarma, Portugal
[email protected]
Elena Rivas Marin
Centro Andaluz de Biología del Desarrollo
CABD, Universidad Pablo de Olavide-CSIC,
Spain
[email protected]
Laura van Niftrik
Institute for Water & Wetland Research,
Faculty of Science, Radboud University, The
Netherlands
[email protected]
Naomi Louise Ward
Departments of Molecular Biology and
Botany, Wyoming INBRE Bioinformatics
Core, USA
[email protected]
Inês Vitorino
FCUP, University of Porto, Portugal
[email protected]
Sandra Wiegand
Faculty of Science, Radboud University
Nijmegen, The Netherlands
[email protected]
29