publication . Article . 2016

The Microbiome and Occurrence of Methanotrophy in Carnivorous Sponges

Jon Thomassen Hestetun; Jon Thomassen Hestetun; Håkon Dahle; Steffen Leth Jørgensen; Bernt Rydland Olsen; Bernt Rydland Olsen; Hans Tore Rapp; Hans Tore Rapp; Hans Tore Rapp;
Open Access English
  • Published: 09 Nov 2016 Journal: Frontiers in Microbiology (issn: 1664-302X, Copyright policy)
  • Publisher: Frontiers Media S.A.
  • Country: Norway
Abstract
As shown by recent studies, filter-feeding sponges are known to host a wide variety of microorganisms. However, the microbial community of the non-filtering carnivorous sponges (Porifera, Cladorhizidae) has been the subject of less scrutiny. Here, we present the results from a comparative study of the methanotrophic carnivorous sponge Cladorhiza methanophila from a mud volcano-rich area at the Barbados Accretionary Prism, and five carnivorous species from the Jan Mayen Vent Field (JMVF) at the Arctic Mid-Ocean Ridge. Results from 16S rRNA microbiome data indicate the presence of a diverse assemblage of associated microorganisms in carnivorous sponges mainly from...
Subjects
free text keywords: European Union, Horizon 2020, Grant Agreement No 679849, Deep-sea Sponge Grounds Ecosystems of the North Atlantic an integrated approach towards their preservation and sustainable exploitation, SponGES, Barbados, Porifera, methane seep, hydrothermal vent, isotope, Cladorhizidae, Microbiology, QR1-502, Original Research, Arctic Mid-Ocean Ridge, Cladorhiza methanophila, Microbiology (medical), Gammaproteobacteria, biology.organism_classification, biology, Thaumarchaeota, Alphaproteobacteria, Sponge, Symbiosis, Microbiome, Ecology, Cladorhiza, food.ingredient, food
Related Organizations
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
,
NSF| Collaborative Research: Connectivity in western Atlantic seep populations: Oceanographic and life-history processes underlying genetic structure
Project
  • Funder: National Science Foundation (NSF)
  • Project Code: 1031050
  • Funding stream: Directorate for Geosciences | Division of Ocean Sciences
70 references, page 1 of 5

Anantharaman K.Breier J. A.Sheik C. S.Dick G. J. (2013). Evidence for hydrogen oxidation and metabolic plasticity in widespread deep-sea sulfur-oxidizing bacteria. Proc. Natl. Acad. Sci. U.S.A. 110 330–335. 10.1073/pnas.1215340110 23263870 [OpenAIRE] [PubMed] [DOI]

Arellano S. M.Lee O. O.Lafi F. F.Yang J.Wang Y.Young C. M. (2013). Deep sequencing of Myxilla (Ectyomyxilla) methanophila, an epibiotic sponge on cold-seep tubeworms, reveals methylotrophic, thiotrophic, and putative hydrocarbon-degrading microbial associations. Microb. Ecol. 65 450–461. 10.1007/s00248-012-0130-y 23052927 [OpenAIRE] [PubMed] [DOI]

Baumberger T. (2011). Volatiles in Marine Hydrothermal Systems. Ph.D. Dissertation, Eidgenössische Technische Hochschule Zürich.

Bergquist P. R. (1978). Sponges. Los Angeles, CA: University of California Press.

Bowman J. P. (2005). “Methylococcales ord. nov,” in Bergey’s Manual of Systematic Bacteriology: The Proteobacteria. Part B The Gamma proteobacteria Vol. 2 eds Brenner D. J.Krieg N. R.Staley J. T.Garrity G. M.Boone D. R.Vos P. D. (Boston, MA: Springer), 248–270.

Caporaso J. G.Kuczynski J.Stombaugh J.Bittinger K.Bushman F. D.Costello E. K. (2010). QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7 335–336. 10.1038/nmeth.f.303 20383131 [OpenAIRE] [PubMed] [DOI]

Carter H. J. (1876). Descriptions and Figures of Deep-Sea Sponges and their Spicules, from the Atlantic Ocean, dredged up on board H.M.S. ‘Porcupine’, chiefly in 1869 (concluded). Ann. Magazine Nat. His. 18 458–479.

Cavanaugh C. M.Levering P. R.Maki J. S.Mitchell R.Lidstrom M. E. (1987). Symbiosis of methylotrophic bacteria and deep-sea mussels. Nature 325 346–348. 10.1038/325346a0 [OpenAIRE] [DOI]

Childress J. J.Fisher C.Brooks J.Kennicutt M.Bidigare R.Anderson A. (1986). A methanotrophic marine molluscan (Bivalvia, Mytilidae) symbiosis: mussels fueled by gas. Science 233 1306–1308. 10.1126/science.233.4770.1306 17843358 [OpenAIRE] [PubMed] [DOI]

Dahle H.Økland I.Thorseth I. H.Pedersen R. B.Steen I. H. (2015). Energy landscapes shape microbial communities in hydrothermal systems on the arctic mid-ocean ridge. ISME J. 9 1593–1606. 10.1038/ismej.2014.247 25575309 [OpenAIRE] [PubMed] [DOI]

Dendy A. (1922). No. I.—The percy sladen trust expedition to the Indian Ocean in 1905, under the leadership of Mr. J. Stanley Gardiner, M.A. Volume VII. No. I.—Report on the Sigmatotetraxonida collected by H.M.S. “Sealark” in the Indian Ocean. Trans. Linn. Soc. Lond. 18 1–164. 10.1111/j.1096-3642.1922.tb00547.x [OpenAIRE] [DOI]

Dupont S.Carre-Mlouka A.Domart-Coulon I.Vacelet J.Bourguet-Kondracki M.-L. (2014). Exploring cultivable bacteria from the prokaryotic community associated with the carnivorous sponge Asbestopluma hypogea. FEMS Microbiol. Ecol. 88 160–174. 10.1111/1574-6941.12279 24392789 [OpenAIRE] [PubMed] [DOI]

Dupont S.Corre E.Li Y.Vacelet J.Bourguet-Kondracki M.-L. (2013). First insights into the m icrobiome of a carnivorous sponge. FEMS Microbiol. Ecol. 86 520–531. 10.1111/1574-6941.12178 23845054 [OpenAIRE] [PubMed] [DOI]

Edgar R. C. (2013). UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10 996–998. 10.1038/nmeth.2604 23955772 [OpenAIRE] [PubMed] [DOI]

Felbeck H. (1981). Chemoautotrophic potential of the hydrothermal vent tube worm, Riftia pachyptila Jones (Vestimentifera). Science 213 336–338. 10.1126/science.213.4505.336 17819905 [OpenAIRE] [PubMed] [DOI]

70 references, page 1 of 5
Abstract
As shown by recent studies, filter-feeding sponges are known to host a wide variety of microorganisms. However, the microbial community of the non-filtering carnivorous sponges (Porifera, Cladorhizidae) has been the subject of less scrutiny. Here, we present the results from a comparative study of the methanotrophic carnivorous sponge Cladorhiza methanophila from a mud volcano-rich area at the Barbados Accretionary Prism, and five carnivorous species from the Jan Mayen Vent Field (JMVF) at the Arctic Mid-Ocean Ridge. Results from 16S rRNA microbiome data indicate the presence of a diverse assemblage of associated microorganisms in carnivorous sponges mainly from...
Subjects
free text keywords: European Union, Horizon 2020, Grant Agreement No 679849, Deep-sea Sponge Grounds Ecosystems of the North Atlantic an integrated approach towards their preservation and sustainable exploitation, SponGES, Barbados, Porifera, methane seep, hydrothermal vent, isotope, Cladorhizidae, Microbiology, QR1-502, Original Research, Arctic Mid-Ocean Ridge, Cladorhiza methanophila, Microbiology (medical), Gammaproteobacteria, biology.organism_classification, biology, Thaumarchaeota, Alphaproteobacteria, Sponge, Symbiosis, Microbiome, Ecology, Cladorhiza, food.ingredient, food
Related Organizations
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
,
NSF| Collaborative Research: Connectivity in western Atlantic seep populations: Oceanographic and life-history processes underlying genetic structure
Project
  • Funder: National Science Foundation (NSF)
  • Project Code: 1031050
  • Funding stream: Directorate for Geosciences | Division of Ocean Sciences
70 references, page 1 of 5

Anantharaman K.Breier J. A.Sheik C. S.Dick G. J. (2013). Evidence for hydrogen oxidation and metabolic plasticity in widespread deep-sea sulfur-oxidizing bacteria. Proc. Natl. Acad. Sci. U.S.A. 110 330–335. 10.1073/pnas.1215340110 23263870 [OpenAIRE] [PubMed] [DOI]

Arellano S. M.Lee O. O.Lafi F. F.Yang J.Wang Y.Young C. M. (2013). Deep sequencing of Myxilla (Ectyomyxilla) methanophila, an epibiotic sponge on cold-seep tubeworms, reveals methylotrophic, thiotrophic, and putative hydrocarbon-degrading microbial associations. Microb. Ecol. 65 450–461. 10.1007/s00248-012-0130-y 23052927 [OpenAIRE] [PubMed] [DOI]

Baumberger T. (2011). Volatiles in Marine Hydrothermal Systems. Ph.D. Dissertation, Eidgenössische Technische Hochschule Zürich.

Bergquist P. R. (1978). Sponges. Los Angeles, CA: University of California Press.

Bowman J. P. (2005). “Methylococcales ord. nov,” in Bergey’s Manual of Systematic Bacteriology: The Proteobacteria. Part B The Gamma proteobacteria Vol. 2 eds Brenner D. J.Krieg N. R.Staley J. T.Garrity G. M.Boone D. R.Vos P. D. (Boston, MA: Springer), 248–270.

Caporaso J. G.Kuczynski J.Stombaugh J.Bittinger K.Bushman F. D.Costello E. K. (2010). QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7 335–336. 10.1038/nmeth.f.303 20383131 [OpenAIRE] [PubMed] [DOI]

Carter H. J. (1876). Descriptions and Figures of Deep-Sea Sponges and their Spicules, from the Atlantic Ocean, dredged up on board H.M.S. ‘Porcupine’, chiefly in 1869 (concluded). Ann. Magazine Nat. His. 18 458–479.

Cavanaugh C. M.Levering P. R.Maki J. S.Mitchell R.Lidstrom M. E. (1987). Symbiosis of methylotrophic bacteria and deep-sea mussels. Nature 325 346–348. 10.1038/325346a0 [OpenAIRE] [DOI]

Childress J. J.Fisher C.Brooks J.Kennicutt M.Bidigare R.Anderson A. (1986). A methanotrophic marine molluscan (Bivalvia, Mytilidae) symbiosis: mussels fueled by gas. Science 233 1306–1308. 10.1126/science.233.4770.1306 17843358 [OpenAIRE] [PubMed] [DOI]

Dahle H.Økland I.Thorseth I. H.Pedersen R. B.Steen I. H. (2015). Energy landscapes shape microbial communities in hydrothermal systems on the arctic mid-ocean ridge. ISME J. 9 1593–1606. 10.1038/ismej.2014.247 25575309 [OpenAIRE] [PubMed] [DOI]

Dendy A. (1922). No. I.—The percy sladen trust expedition to the Indian Ocean in 1905, under the leadership of Mr. J. Stanley Gardiner, M.A. Volume VII. No. I.—Report on the Sigmatotetraxonida collected by H.M.S. “Sealark” in the Indian Ocean. Trans. Linn. Soc. Lond. 18 1–164. 10.1111/j.1096-3642.1922.tb00547.x [OpenAIRE] [DOI]

Dupont S.Carre-Mlouka A.Domart-Coulon I.Vacelet J.Bourguet-Kondracki M.-L. (2014). Exploring cultivable bacteria from the prokaryotic community associated with the carnivorous sponge Asbestopluma hypogea. FEMS Microbiol. Ecol. 88 160–174. 10.1111/1574-6941.12279 24392789 [OpenAIRE] [PubMed] [DOI]

Dupont S.Corre E.Li Y.Vacelet J.Bourguet-Kondracki M.-L. (2013). First insights into the m icrobiome of a carnivorous sponge. FEMS Microbiol. Ecol. 86 520–531. 10.1111/1574-6941.12178 23845054 [OpenAIRE] [PubMed] [DOI]

Edgar R. C. (2013). UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10 996–998. 10.1038/nmeth.2604 23955772 [OpenAIRE] [PubMed] [DOI]

Felbeck H. (1981). Chemoautotrophic potential of the hydrothermal vent tube worm, Riftia pachyptila Jones (Vestimentifera). Science 213 336–338. 10.1126/science.213.4505.336 17819905 [OpenAIRE] [PubMed] [DOI]

70 references, page 1 of 5
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