Metagenomic binning of a marine sponge microbiome reveals unity in defense but metabolic specialization

Slaby, Beate M.; Hackl, Thomas; Horn, Hannes; Bayer, Kristina; Hentschel, Ute

doi:10.1038/ismej.2017.101

Metagenomic binning of a marine sponge microbiome reveals unity in defense but metabolic specialization

Journal Article · Tue Jul 11 00:00:00 EDT 2017 · The ISME Journal

DOI:https://doi.org/10.1038/ismej.2017.101· OSTI ID:1623776

^[1]; Hackl, Thomas ^[2]; Horn, Hannes ^[3]; Bayer, Kristina ^[4]; Hentschel, Ute ^[5]

GEOMAR Helmholtz Centre for Ocean Research Kiel (Germany). RD3 Marine Microbiology; Univ. of Wurzburg (Germany). Julius-von-Sachs Inst. for Biological Science. Dept. of Botany II; DOE/OSTI
Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States). Dept. of Civil and Environmental Engineering
GEOMAR Helmholtz Centre for Ocean Research Kiel (Germany). RD3 Marine Microbiology; Univ. of Wurzburg (Germany). Julius-von-Sachs Inst. for Biological Science. Dept. of Botany II
GEOMAR Helmholtz Centre for Ocean Research Kiel (Germany). RD3 Marine Microbiology
GEOMAR Helmholtz Centre for Ocean Research Kiel (Germany). RD3 Marine Microbiology; Christian-Albrechts Univ. of Kiel (Germany)

Marine sponges are ancient metazoans that are populated by distinct and highly diverse microbial communities. In order to obtain deeper insights into the functional gene repertoire of the Mediterranean sponge Aplysina aerophoba, we combined Illumina short-read and PacBio long-read sequencing followed by un-targeted metagenomic binning. We identified a total of 37 high-quality bins representing 11 bacterial phyla and two candidate phyla. Statistical comparison of symbiont genomes with selected reference genomes revealed a significant enrichment of genes related to bacterial defense (restriction-modification systems, toxin-antitoxin systems) as well as genes involved in host colonization and extracellular matrix utilization in sponge symbionts. A within-symbionts genome comparison revealed a nutritional specialization of at least two symbiont guilds, where one appears to metabolize carnitine and the other sulfated polysaccharides, both of which are abundant molecules in the sponge extracellular matrix. A third guild of symbionts may be viewed as nutritional generalists that perform largely the same metabolic pathways but lack such extraordinary numbers of the relevant genes. This study characterizes the genomic repertoire of sponge symbionts at an unprecedented resolution and it provides greater insights into the molecular mechanisms underlying microbial-sponge symbiosis.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1623776

Journal Information:: The ISME Journal, Journal Name: The ISME Journal Journal Issue: 11 Vol. 11; ISSN 1751-7362

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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Life at Home and on the Roam: Genomic Adaptions Reflect the Dual Lifestyle of an Intracellular, Facultative Symbiont Burgsdorf, Ilia; Handley, Kim M.; Bar-Shalom, Rinat mSystems, Vol. 4, Issue 4 https://doi.org/10.1128/msystems.00057-19	journal	May 2019
The sponge holobiont in a changing ocean: from microbes to ecosystems Pita, L.; Rix, L.; Slaby, B. M. Microbiome, Vol. 6, Issue 1 https://doi.org/10.1186/s40168-018-0428-1	journal	March 2018
Bacterial Exposure Mediates Developmental Plasticity and Resistance to Lethal Vibrio lentus Infection in Purple Sea Urchin (Strongylocentrotus purpuratus) Larvae Schuh, Nicholas W.; Carrier, Tyler J.; Schrankel, Catherine S. Frontiers in Immunology, Vol. 10 https://doi.org/10.3389/fimmu.2019.03014	journal	January 2020
Metagenomics Investigation of Agarlytic Genes and Genomes in Mangrove Sediments in China: A Potential Repertory for Carbohydrate-Active Enzymes Qu, Wu; Lin, Dan; Zhang, Zhouhao Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.01864	journal	August 2018
Comparative Genomics of Marine Sponge-Derived Streptomyces spp. Isolates SM17 and SM18 With Their Closest Terrestrial Relatives Provides Novel Insights Into Environmental Niche Adaptations and Secondary Metabolite Biosynthesis Potential Almeida, Eduardo L.; Carrillo Rincón, Andrés Felipe; Jackson, Stephen A. Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.01713	journal	July 2019
The ecology of killer yeasts: Interference competition in natural habitats Boynton, Primrose J. Yeast, Vol. 36, Issue 8 https://doi.org/10.1002/yea.3398	journal	June 2019
Pangenomic comparison of globally distributed Poribacteria associated with sponge hosts and marine particles Podell, Sheila; Blanton, Jessica M.; Neu, Alexander The ISME Journal, Vol. 13, Issue 2 https://doi.org/10.1038/s41396-018-0292-9	journal	October 2018
Fueled by methane: deep-sea sponges from asphalt seeps gain their nutrition from methane-oxidizing symbionts Rubin-Blum, Maxim; Antony, Chakkiath Paul; Sayavedra, Lizbeth The ISME Journal, Vol. 13, Issue 5 https://doi.org/10.1038/s41396-019-0346-7	journal	January 2019
Characterization of a sponge microbiome using an integrative genome-centric approach Engelberts, J. Pamela; Robbins, Steven J.; de Goeij, Jasper M. The ISME Journal, Vol. 14, Issue 5 https://doi.org/10.1038/s41396-020-0591-9	journal	January 2020
Archaeal communities in sponge, sediment and water from marine lakes and open water habitats Polónia, Ana Rita Moura; Cleary, Daniel Francis Richard Marine Biology Research, Vol. 15, Issue 3 https://doi.org/10.1080/17451000.2019.1633469	journal	March 2019
Current challenges and best-practice protocols for microbiome analysis Bharti, Richa; Grimm, Dominik G. Briefings in Bioinformatics https://doi.org/10.1093/bib/bbz155	journal	December 2019
Metagenomic binning reveals versatile nutrient cycling and distinct adaptive features in alphaproteobacterial symbionts of marine sponges Karimi, Elham; Slaby, Beate M.; Soares, André R. FEMS Microbiology Ecology, Vol. 94, Issue 6 https://doi.org/10.1093/femsec/fiy074	journal	April 2018
Bacterial diversity in the marine sponge Halichondria panicea from Icelandic waters and host-specificity of its dominant symbiont “ Candidatus Halichondribacter symbioticus” Knobloch, Stephen; Jóhannsson, Ragnar; Marteinsson, Viggó FEMS Microbiology Ecology, Vol. 95, Issue 1 https://doi.org/10.1093/femsec/fiy220	journal	November 2018
Phylogeny and genomics of SAUL, an enigmatic bacterial lineage frequently associated with marine sponges: Phylogeny and genomics of SAUL Astudillo-García, Carmen; Slaby, Beate M.; Waite, David W. Environmental Microbiology, Vol. 20, Issue 2 https://doi.org/10.1111/1462-2920.13965	journal	November 2017
In situ meta‐omic insights into the community compositions and ecological roles of hadal microbes in the Mariana Trench Gao, Zhao‐Ming; Huang, Jiao‐Mei; Cui, Guo‐Jie Environmental Microbiology, Vol. 21, Issue 11 https://doi.org/10.1111/1462-2920.14759	journal	August 2019
Genome analysis of sponge symbiont ‘ Candidatus Halichondribacter symbioticus’ shows genomic adaptation to a host‐dependent lifestyle Knobloch, Stephen; Jóhannsson, Ragnar; Marteinsson, Viggó Þór Environmental Microbiology, Vol. 22, Issue 1 https://doi.org/10.1111/1462-2920.14869	journal	November 2019
Potential Interactions between Clade SUP05 Sulfur-Oxidizing Bacteria and Phages in Hydrothermal Vent Sponges Zhou, Kun; Zhang, Rui; Sun, Jin Applied and Environmental Microbiology, Vol. 85, Issue 22 https://doi.org/10.1128/AEM.00992-19	journal	November 2019
Pangenomics Analysis Reveals Diversification of Enzyme Families and Niche Specialization in Globally Abundant SAR202 Bacteria Saw, Jimmy H. W.; Nunoura, Takuro; Hirai, Miho mBio, Vol. 11, Issue 1 https://doi.org/10.1128/mBio.02975-19	journal	January 2020
Comparative Genomics of Cyanobacterial Symbionts Reveals Distinct, Specialized Metabolism in Tropical Dysideidae Sponges Schorn, Michelle A.; Jordan, Peter A.; Podell, Sheila mBio, Vol. 10, Issue 3 https://doi.org/10.1128/mbio.00821-19	journal	May 2019
Marine Sponges as Chloroflexi Hot Spots: Genomic Insights and High-Resolution Visualization of an Abundant and Diverse Symbiotic Clade Bayer, Kristina; Jahn, Martin T.; Slaby, Beate M. mSystems, Vol. 3, Issue 6 https://doi.org/10.1128/msystems.00150-18	journal	December 2018
Prokaryotic Diversity and Community Patterns in Antarctic Continental Shelf Sponges Steinert, Georg; Wemheuer, Bernd; Janussen, Dorte Frontiers in Marine Science, Vol. 6 https://doi.org/10.3389/fmars.2019.00297	journal	June 2019
Comparative Metagenomics Reveals the Distinctive Adaptive Features of the Spongia officinalis Endosymbiotic Consortium Karimi, Elham; Ramos, Miguel; Gonçalves, Jorge M. S. Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.02499	journal	December 2017
Cultivation of Sponge-Associated Bacteria from Agelas sventres and Xestospongia muta Collected from Different Depths Indraningrat, Anak; Micheller, Sebastian; Runderkamp, Mandy Marine Drugs, Vol. 17, Issue 10 https://doi.org/10.3390/md17100578	journal	October 2019
Impact of the Cultivation Technique on the Production of Secondary Metabolites by Chrysosporium lobatum TM-237-S5, Isolated from the Sponge Acanthella cavernosa Le Goff, Géraldine; Lopes, Philippe; Arcile, Guillaume Marine Drugs, Vol. 17, Issue 12 https://doi.org/10.3390/md17120678	journal	November 2019
Pangenomics Analysis Reveals Diversification of Enzyme Families and Niche Specialization in Globally Abundant SAR202 Bacteria Saw, Jimmy H. W.; Nunoura, Takuro; Hirai, Miho ETH Zurich https://doi.org/10.3929/ethz-b-000391789	text	January 2020

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