Cited by 276Marine Sponges and Natural ProductsMicrobial Community Ecology and PhysiologyGenomics and Phylogenetic Studies

Single-cell genomics reveals the lifestyle of Poribacteria , a candidate phylum symbiotically associated with marine sponges

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Siegl, Alexander, Kamke, Janine, Hochmuth, Thomas, Piel, Jörn, Richter, Michael, Liang, Chunguang, Dandekar, Thomas, Hentschel, Ute·2011·The ISME Journal

Abstract

In this study, we present a single-cell genomics approach for the functional characterization of the candidate phylum Poribacteria, members of which are nearly exclusively found in marine sponges. The microbial consortia of the Mediterranean sponge Aplysina aerophoba were singularized by fluorescence-activated cell sorting, and individual microbial cells were subjected to phi29 polymerase-mediated ‘whole-genome amplification’. Pyrosequencing of a single amplified genome (SAG) derived from a member of the Poribacteria resulted in nearly 1.6 Mb of genomic information distributed among 554 contigs analyzed in this study. Approximately two-third of the poribacterial genome was sequenced. Our findings shed light on the functional properties and lifestyle of a possibly ancient bacterial symbiont of marine sponges. The Poribacteria are mixotrophic bacteria with autotrophic CO2-fixation capacities through the Wood–Ljungdahl pathway. The cell wall is of Gram-negative origin. The Poribacteria produce at least two polyketide synthases (PKSs), one of which is the sponge-specific Sup-type PKS. Several putative symbiosis factors such as adhesins (bacterial Ig-like domains, lamininin G domain proteins), adhesin-related proteins (ankyrin, fibronectin type III) and tetratrico peptide repeat domain-encoding proteins were identified, which might be involved in mediating sponge–microbe interactions. The discovery of genes coding for 24-isopropyl steroids implies that certain fossil biomarkers used to date the origins of metazoan life on earth may possibly be of poribacterial origin. Single-cell genomic approaches, such as those shown herein, contribute to a better understanding of beneficial microbial consortia, of which most members are, because of the lack of cultivation, inaccessible by conventional techniques.

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  • Older records of animals are controversial.

    “Older records of animals are controversial: organic biomarkers indicative of demosponges [20] are apparently derived ultimately from now symbiotic bacteria [21]; putative animal embryo fossils [22] are alternately interpreted as protists [23, 24, 25]; and contested reports of sponges [26, 27], molluscs [28], and innumerable cnidarians [29], as well as putative traces of eumetazoan or bilaterian”

    From Uncertainty in the Timing of Origin of Animals and the Limits of Precision in Molecular Timescales (2015) · cites this paper as [21]

    The Sterol biosynthesis section proposes that fossil steroid biomarkers associated with demosponges may originate from Poribacteria, bacteria associated with sponges. It calls this a “fascinating possibility,” so the citing sentence’s assertion that the biomarkers are apparently derived from those bacteria is more certain than the source supports. (LLM, conf=0.88)

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  1. [36]36. Quast C. (2006). MicHanThi-design and implementation of a system for the prediction of gene functions in genome annotation projects. Diploma thesis, University of Bremen.

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Authors
Siegl, A., Kamke, J., Hochmuth, T., Piel, J., Richter, M., Liang, C., Dandekar, T., & Hentschel, U.
Affiliations
  • University of Vienna (AT)
  • University of Würzburg (DE)
  • University of Bonn (DE)
  • Ribocon (Germany) (DE)
Corresponding author
Hentschel, Ute
Venue
The ISME Journal
Published
2010-07-08
Volume
5
Issue
1
Pages
61-70
ISSN
  • 1751-7362 (ISSN-L)
  • 1751-7370
OpenAlex
W2040439966
Cited by
276
References
56
Citations by year
2026: 3 · 2025: 5 · 2024: 12 · 2023: 9 · 2022: 9 · 2021: 21 · 2020: 8 · 2019: 17 · 2018: 24 · 2017: 26 · 2016: 22 · 2015: 19 · 2014: 23 · 2013: 39 · 2012: 21
FWCI
21.21
Type
journal article
Language
en
Open access
Locations
  • The ISME Journal (publishedVersion)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • Helmholtz Centre for Ocean Research Kiel (GEOMAR) (acceptedVersion)
  • Phaidra (Universität Wien) (submittedVersion, cc-by-nc-nd)
  • mediaTUM – the media and publications repository of the Technical University Munich (Technical University Munich) (submittedVersion)
Funders
  • U.S. Department of Energy
  • Joint Genome Institute
  • Deutsche Forschungsgemeinschaft (SFB567, Da 208/10-1)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Biotechnology › Marine Sponges and Natural Products
  • Physical Sciences › Environmental Science › Ecology › Microbial Community Ecology and Physiology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
Keywords
marine sponge symbionts, Aplysina aerophoba, bacterial symbiosis, mixotrophic bacteria, Wood-Ljungdahl pathway, polyketide synthase, adhesins, metazoan origin, microbial consortia, single amplified genomes
MeSH terms
Animals, Bacteria, Molecular Sequence Data, Phylogeny, Porifera, Sterols, Symbiosis, Genome, Bacterial, Bacterial Physiological Phenomena, Genomics, Polyketide Synthases

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