publication . Article . Preprint . Other literature type . 2018

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.; Moitinho-Silva, Lucas; Hentschel, Ute;
Open Access
  • Published: 22 May 2018
  • Publisher: Cold Spring Harbor Laboratory
  • Country: Germany
Abstract
Chloroflexi represent a widespread, yet enigmatic bacterial phylum with few cultivated members. We used metagenomic and single-cell genomic approaches to characterize the functional gene repertoire of Chloroflexi symbionts in marine sponges. The results of this study suggest clade-specific metabolic specialization and that Chloroflexi symbionts have the genomic potential for dissolved organic matter (DOM) degradation from seawater. Considering the abundance and dominance of sponges in many benthic environments, we predict that the role of sponge symbionts in biogeochemical cycles is larger than previously thought.
Subjects
Medical Subject Headings: fungibacteriabiochemical phenomena, metabolism, and nutritionanimal structures
free text keywords: European Union (EU), Horizon 2020, Grant Agreement No 679849, an integrated approach towards their preservation and sustainable exploitation [Deep-sea Sponge Grounds Ecosystems of the North Atlantic], SponGES, Microbiome, Sponge, biology.organism_classification, biology, Evolutionary biology, Phylum, Genome, Metagenomics, Phylogenetic tree, Symbiosis, Secondary metabolite, medicine.drug, medicine, Poribacteria, Genomics, Clade, Gene, Genetics, Chloroflexi, DOM degradation, FISH-CLEM, metabolism, metagenomic binning, single-cell genomics, sponge symbiosis, Microbiology, QR1-502, Research Article, Host-Microbe Biology
Funded by
EC| SponGES
Project
SponGES
Deep-sea Sponge Grounds Ecosystems of the North Atlantic: an integrated approach towards their preservation and sustainable exploitation
  • Funder: European Commission (EC)
  • Project Code: 679849
  • Funding stream: H2020 | RIA
Communities
EuroMarine
European Marine Science
OceanRep
Article . 2018
Provider: OceanRep
mSystems
Article . 2018
Provider: Crossref
mSystems
Article
Provider: UnpayWall
87 references, page 1 of 6

1.Li CW, Chen JY, Hua TE 1998 Precambrian sponges with cellular structures. Science 279:879–882.9452391 [PubMed]

2.Yin Z, Zhu M, Davidson EH, Bottjer DJ, Zhao F, Tafforeau P 2015 Sponge grade body fossil with cellular resolution dating 60 Myr before the Cambrian. Proc Natl Acad Sci U S A 112:E1453–E1460. doi:10.1073/pnas.1414577112.25775601 [OpenAIRE] [PubMed] [DOI]

3.Van Soest RWM, Boury-Esnault N, Vacelet J, Dohrmann M, Erpenbeck D, De Voogd NJ, Santodomingo N, Vanhoorne B, Kelly M, Hooper JNA 2012 Global diversity of sponges (Porifera). PLoS One 7:e35105. doi:10.1371/journal.pone.0035105.22558119 [OpenAIRE] [PubMed] [DOI]

4.Bell JJ 2008 The functional roles of marine sponges. Estuar Coast Shelf Sci 79:341–353. doi:10.1016/j.ecss.2008.05.002. [OpenAIRE] [DOI]

5.Maldonado M, Ribes M, van Duyl FC 2012 Nutrient fluxes through sponges: biology, budgets, and ecological implications. Adv Mar Biol 62:113–182. doi:10.1016/B978-0-12-394283-8.00003-5.22664122 [OpenAIRE] [PubMed] [DOI]

6.Thomas T, Moitinho-Silva L, Lurgi M, Björk JR, Easson C, Astudillo-García C, Olson JB, Erwin PM, López-Legentil S, Luter H, Chaves-Fonnegra A, Costa R, Schupp PJ, Steindler L, Erpenbeck D, Gilbert J, Knight R, Ackermann G, Victor Lopez J, Taylor MW, Thacker RW, Montoya JM, Hentschel U, Webster NS 2016 Diversity, structure and convergent evolution of the global sponge microbiome. Nat Commun 7:11870. doi:10.1038/ncomms11870.27306690 [OpenAIRE] [PubMed] [DOI]

7.McMurray S, Stubler A, Erwin P, Finelli C, Pawlik J 2018 A test of the sponge-loop hypothesis for emergent Caribbean reef sponges. Mar Ecol Prog Ser 588:1–14. doi:10.3354/meps12466. [OpenAIRE] [DOI]

8.Blunt JW, Copp BR, Keyzers RA, Munro MHG, Prinsep MR 2017 Marine natural products. Nat Prod Rep 34:235–294. doi:10.1039/c6np00124f.28290569 [PubMed] [DOI]

9.Wilson MC, Mori T, Rückert C, Uria AR, Helf MJ, Takada K, Gernert C, Steffens UAE, Heycke N, Schmi tt S, Rinke C, Helfrich EJN, Brachmann AO, Gurgui C, Wakimoto T, Kracht M, Crüsemann M, Hentschel U, Abe I, Matsunaga S, Kalinowski J, Takeyama H, Piel J 2014 An environmental bacterial taxon with a large and distinct metabolic repertoire. Nature 506:58–62. doi:10.1038/nature12959.24476823 [OpenAIRE] [PubMed] [DOI]

10.Lackner G, Peters EE, Helfrich EJN, Piel J 2017 Insights into the lifestyle of uncultured bacterial natural product factories associated with marine sponges. Proc Natl Acad Sci U S A 114:E347–E356. doi:10.1073/pnas.1616234114.28049838 [OpenAIRE] [PubMed] [DOI]

11.Hentschel U, Usher KM, Taylor MW 2006 Marine sponges as microbial fermenters. FEMS Microbiol Ecol 55:167–177. doi:10.1111/j.1574-6941.2005.00046.x.16420625 [OpenAIRE] [PubMed] [DOI]

12.Moitinho-Silva L, Steinert G, Nielsen S, Hardoim CCP, Wu YC, McCormack GP, López-Legentil S, Marchant R, Webster N, Thomas T, Hentschel U 2017 Predicting the HMA-LMA status in marine sponges by machine learning. Front Microbiol 8:752. doi:10.3389/fmicb.2017.00752.28533766 [OpenAIRE] [PubMed] [DOI]

13.Pita L, Rix L, Slaby BM, Franke A, Hentschel U 2018 The sponge holobiont in a changing ocean: from microbes to ecosystems. Microbiome 6:46. doi:10.1186/s40168-018-0428-1.29523192 [OpenAIRE] [PubMed] [DOI]

14.Bayer K, Moitinho-Silva L, Brümmer F, Cannistraci CV, Ravasi T, Hentschel U 2014 GeoChip-based insights into the microbial functional gene repertoire of marine sponges (high microbial abundance, low microbial abundance) and seawater. FEMS Microbiol Ecol 90:832–843. doi:10.1111/1574-6941.12441.25318900 [OpenAIRE] [PubMed] [DOI]

15.Weisz JB, Lindquist N, Martens CS 2008 Do associated microbial abundances impact marine demosponge pumping rates and tissue densities?Oecologia 155:367–376. doi:10.1007/s00442-007-0910-0.18030495 [OpenAIRE] [PubMed] [DOI]

87 references, page 1 of 6
Abstract
Chloroflexi represent a widespread, yet enigmatic bacterial phylum with few cultivated members. We used metagenomic and single-cell genomic approaches to characterize the functional gene repertoire of Chloroflexi symbionts in marine sponges. The results of this study suggest clade-specific metabolic specialization and that Chloroflexi symbionts have the genomic potential for dissolved organic matter (DOM) degradation from seawater. Considering the abundance and dominance of sponges in many benthic environments, we predict that the role of sponge symbionts in biogeochemical cycles is larger than previously thought.
Subjects
Medical Subject Headings: fungibacteriabiochemical phenomena, metabolism, and nutritionanimal structures
free text keywords: European Union (EU), Horizon 2020, Grant Agreement No 679849, an integrated approach towards their preservation and sustainable exploitation [Deep-sea Sponge Grounds Ecosystems of the North Atlantic], SponGES, Microbiome, Sponge, biology.organism_classification, biology, Evolutionary biology, Phylum, Genome, Metagenomics, Phylogenetic tree, Symbiosis, Secondary metabolite, medicine.drug, medicine, Poribacteria, Genomics, Clade, Gene, Genetics, Chloroflexi, DOM degradation, FISH-CLEM, metabolism, metagenomic binning, single-cell genomics, sponge symbiosis, Microbiology, QR1-502, Research Article, Host-Microbe Biology
Funded by
EC| SponGES
Project
SponGES
Deep-sea Sponge Grounds Ecosystems of the North Atlantic: an integrated approach towards their preservation and sustainable exploitation
  • Funder: European Commission (EC)
  • Project Code: 679849
  • Funding stream: H2020 | RIA
Communities
EuroMarine
European Marine Science
OceanRep
Article . 2018
Provider: OceanRep
mSystems
Article . 2018
Provider: Crossref
mSystems
Article
Provider: UnpayWall
87 references, page 1 of 6

1.Li CW, Chen JY, Hua TE 1998 Precambrian sponges with cellular structures. Science 279:879–882.9452391 [PubMed]

2.Yin Z, Zhu M, Davidson EH, Bottjer DJ, Zhao F, Tafforeau P 2015 Sponge grade body fossil with cellular resolution dating 60 Myr before the Cambrian. Proc Natl Acad Sci U S A 112:E1453–E1460. doi:10.1073/pnas.1414577112.25775601 [OpenAIRE] [PubMed] [DOI]

3.Van Soest RWM, Boury-Esnault N, Vacelet J, Dohrmann M, Erpenbeck D, De Voogd NJ, Santodomingo N, Vanhoorne B, Kelly M, Hooper JNA 2012 Global diversity of sponges (Porifera). PLoS One 7:e35105. doi:10.1371/journal.pone.0035105.22558119 [OpenAIRE] [PubMed] [DOI]

4.Bell JJ 2008 The functional roles of marine sponges. Estuar Coast Shelf Sci 79:341–353. doi:10.1016/j.ecss.2008.05.002. [OpenAIRE] [DOI]

5.Maldonado M, Ribes M, van Duyl FC 2012 Nutrient fluxes through sponges: biology, budgets, and ecological implications. Adv Mar Biol 62:113–182. doi:10.1016/B978-0-12-394283-8.00003-5.22664122 [OpenAIRE] [PubMed] [DOI]

6.Thomas T, Moitinho-Silva L, Lurgi M, Björk JR, Easson C, Astudillo-García C, Olson JB, Erwin PM, López-Legentil S, Luter H, Chaves-Fonnegra A, Costa R, Schupp PJ, Steindler L, Erpenbeck D, Gilbert J, Knight R, Ackermann G, Victor Lopez J, Taylor MW, Thacker RW, Montoya JM, Hentschel U, Webster NS 2016 Diversity, structure and convergent evolution of the global sponge microbiome. Nat Commun 7:11870. doi:10.1038/ncomms11870.27306690 [OpenAIRE] [PubMed] [DOI]

7.McMurray S, Stubler A, Erwin P, Finelli C, Pawlik J 2018 A test of the sponge-loop hypothesis for emergent Caribbean reef sponges. Mar Ecol Prog Ser 588:1–14. doi:10.3354/meps12466. [OpenAIRE] [DOI]

8.Blunt JW, Copp BR, Keyzers RA, Munro MHG, Prinsep MR 2017 Marine natural products. Nat Prod Rep 34:235–294. doi:10.1039/c6np00124f.28290569 [PubMed] [DOI]

9.Wilson MC, Mori T, Rückert C, Uria AR, Helf MJ, Takada K, Gernert C, Steffens UAE, Heycke N, Schmi tt S, Rinke C, Helfrich EJN, Brachmann AO, Gurgui C, Wakimoto T, Kracht M, Crüsemann M, Hentschel U, Abe I, Matsunaga S, Kalinowski J, Takeyama H, Piel J 2014 An environmental bacterial taxon with a large and distinct metabolic repertoire. Nature 506:58–62. doi:10.1038/nature12959.24476823 [OpenAIRE] [PubMed] [DOI]

10.Lackner G, Peters EE, Helfrich EJN, Piel J 2017 Insights into the lifestyle of uncultured bacterial natural product factories associated with marine sponges. Proc Natl Acad Sci U S A 114:E347–E356. doi:10.1073/pnas.1616234114.28049838 [OpenAIRE] [PubMed] [DOI]

11.Hentschel U, Usher KM, Taylor MW 2006 Marine sponges as microbial fermenters. FEMS Microbiol Ecol 55:167–177. doi:10.1111/j.1574-6941.2005.00046.x.16420625 [OpenAIRE] [PubMed] [DOI]

12.Moitinho-Silva L, Steinert G, Nielsen S, Hardoim CCP, Wu YC, McCormack GP, López-Legentil S, Marchant R, Webster N, Thomas T, Hentschel U 2017 Predicting the HMA-LMA status in marine sponges by machine learning. Front Microbiol 8:752. doi:10.3389/fmicb.2017.00752.28533766 [OpenAIRE] [PubMed] [DOI]

13.Pita L, Rix L, Slaby BM, Franke A, Hentschel U 2018 The sponge holobiont in a changing ocean: from microbes to ecosystems. Microbiome 6:46. doi:10.1186/s40168-018-0428-1.29523192 [OpenAIRE] [PubMed] [DOI]

14.Bayer K, Moitinho-Silva L, Brümmer F, Cannistraci CV, Ravasi T, Hentschel U 2014 GeoChip-based insights into the microbial functional gene repertoire of marine sponges (high microbial abundance, low microbial abundance) and seawater. FEMS Microbiol Ecol 90:832–843. doi:10.1111/1574-6941.12441.25318900 [OpenAIRE] [PubMed] [DOI]

15.Weisz JB, Lindquist N, Martens CS 2008 Do associated microbial abundances impact marine demosponge pumping rates and tissue densities?Oecologia 155:367–376. doi:10.1007/s00442-007-0910-0.18030495 [OpenAIRE] [PubMed] [DOI]

87 references, page 1 of 6
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publication . Article . Preprint . Other literature type . 2018

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.; Moitinho-Silva, Lucas; Hentschel, Ute;