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Single-cell genomics reveals the lifestyle of Poribacteria , a candidate phylum symbiotically associated with marine sponges
Open accessAbstract
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: 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]
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Rappé, M. S., & Giovannoni, S. J. (2003) · Annual Review of Microbiology · doi:10.1146/annurev.micro.57.030502.090759 · Cited by 2,017
Sponge-Associated Microorganisms: Evolution, Ecology, and Biotechnological Potential
Taylor, M. W., Radax, R., Steger, D., & Wagner, M. (2007) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00040-06 · Cited by 1,493
Comprehensive human genome amplification using multiple displacement amplification
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Acetogenesis and the Wood–Ljungdahl pathway of CO2 fixation
Ragsdale, S. W., & Pierce, E. (2008) · Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics · doi:10.1016/j.bbapap.2008.08.012 · Cited by 1,409
MetaGene: prokaryotic gene finding from environmental genome shotgun sequences
Noguchi, H., Park, J., & Takagi, T. (2006) · Nucleic Acids Research · doi:10.1093/nar/gkl723 · Cited by 1,156
Database resources of the National Center for Biotechnology
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Dean, F. B., Nelson, J. R., Giesler, T. L., & Lasken, R. S. (2001) · Genome Research · doi:10.1101/gr.180501 · Cited by 1,070
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- Lasken, 2005, Whole Genome Amplification: Methods Express, 119
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Animals in a bacterial world, a new imperative for the life sciences
McFall‐Ngai, M., Hadfield, M. G., Bosch, T. C. G., Carey, H. V., Domazet‐Lošo, T., Douglas, A. E., Dubilier, N., Eberl, G., Fukami, T., Gilbert, S. F., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1218525110 · Cited by 2,879
Self-citationZhou, Z., Tran, P. Q., Breister, A. M., Liu, Y., Kieft, K., Cowley, E. S., Karaöz, U., & Anantharaman, K. (2022) · Microbiome · doi:10.1186/s40168-021-01213-8 · Cited by 662
Genomic insights into the marine sponge microbiome
Hentschel, U., Piel, J., Degnan, S. M., & Taylor, M. W. (2012) · Nature Reviews Microbiology · doi:10.1038/nrmicro2839 · Cited by 659
Self-citationMarine sponges and their microbial symbionts: love and other relationships
Webster, N. S., & Taylor, M. W. (2011) · Environmental Microbiology · doi:10.1111/j.1462-2920.2011.02460.x · Cited by 658
An environmental bacterial taxon with a large and distinct metabolic repertoire
Wilson, M. C., Mori, T., Rückert, C., Uria, A. R., Helf, M. J., Takada, K., Gernert, C., Steffens, U. A. E., Heycke, N., Schmitt, S., et al. (2014) · Nature · doi:10.1038/nature12959 · Cited by 612
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Metadata
- 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
- Publisher
- Oxford University Press (OUP)
- Published
- 2010-07-08
- Volume
- 5
- Issue
- 1
- Pages
- 61-70
- ISSN
- 1751-7362 (ISSN-L)
- 1751-7370
- PMC
- PMC3105677
- 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
- bronze
- doi.org
- 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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