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Methanotrophic bacterial symbionts fuel dense populations of deep-sea feather duster worms (Sabellida, Annelida) and extend the spatial influence of methane seepage

Goffredi, Shana K. and Tilic, Ekin and Mullin, Sean W. and Dawson, Katherine S. and Keller, Abigail and Lee, Raymond W. and Wu, Fabai and Levin, Lisa A. and Rouse, Greg W. and Cordes, Erik E. and Orphan, Victoria J. (2020) Methanotrophic bacterial symbionts fuel dense populations of deep-sea feather duster worms (Sabellida, Annelida) and extend the spatial influence of methane seepage. Science Advances, 6 (14). Art. No. eaay8562. ISSN 2375-2548. https://resolver.caltech.edu/CaltechAUTHORS:20200102-085056769

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Abstract

Deep-sea cold seeps are dynamic sources of methane release and unique habitats supporting ocean biodiversity and productivity. Here, we describe newly discovered animal-bacterial symbioses fueled by methane, between two species of annelid (a serpulid Laminatubus and sabellid Bispira) and distinct aerobic methane-oxidizing bacteria belonging to the Methylococcales, localized to the host respiratory crown. Worm tissue δ¹³C of −44 to −58‰ are consistent with methane-fueled nutrition for both species, and shipboard stable isotope labeling experiments revealed active assimilation of ¹³C-labeled methane into animal biomass, which occurs via the engulfment of methanotrophic bacteria across the crown epidermal surface. These worms represent a new addition to the few animals known to intimately associate with methane-oxidizing bacteria and may further explain their enigmatic mass occurrence at 150–million year–old fossil seeps. High-resolution seafloor surveys document significant coverage by these symbioses, beyond typical obligate seep fauna. These findings uncover novel consumers of methane in the deep sea and, by expanding the known spatial extent of methane seeps, may have important implications for deep-sea conservation.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1126/sciadv.aay8562DOIArticle
https://advances.sciencemag.org/content/6/14/eaay8562/suppl/DC1PublisherSupporting Information
https://doi.org/10.1101/2019.12.23.887653DOIDiscussion Paper
https://doi.org/10.5061/dryad.wdbrv15jqDOIraw Illumina 16S rRNA barcode sequences and metadata collected in this study
https://sioapps.ucsd.edu/collections/bi/Related ItemBenthic Invertebrate Collection
ORCID:
AuthorORCID
Goffredi, Shana K.0000-0002-9110-9591
Dawson, Katherine S.0000-0001-8856-4609
Wu, Fabai0000-0001-5812-5621
Levin, Lisa A.0000-0002-2858-8622
Orphan, Victoria J.0000-0002-5374-6178
Alternate Title:Sequestration of Methane by Symbiotic Deep-Sea Annelids: Ancient and Future Implications of Redefining the Seep Influence
Additional Information:© 2020 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution NonCommercial License 4.0 (CC BY-NC). Received for publication July 24, 2019. Accepted for publication January 9, 2020. We thank the captains and crew of the R/V Atlantis, HOV Alvin pilots and technicians, AUV Sentry team, as well as scientific participants of AT37-13 and AT42-03, especially O. Pereira, L. McCormick, C. Seid, and A. Durkin, for their assistance at sea. We also thank the captain and crew of the R/V Falkor, ROV SuBastian pilots and technicians, scientific participants of FK190106, as well as J. Gonzalez, A. Crémière, J. Magyar, and S. Connon for their assistance and contributions to the isotope, ion chromatography, nanoSIMS, and microbial community analysis, respectively. C. Roman (University of Rhode Island, as co–principal investigator) and J. Cortes Nunez (University of Costa Rica, international collaborator) played significant roles as co–principal investigators during both expeditions and contributed current meter data. In addition, Occidental College undergraduates M. Cazin, K. Ruis, and C. Brzechffa assisted with microbial community and microscopy analysis, sponsored by the Oxy Undergraduate Research Center. Funding: Support for S.K.G. was provided by a Faculty Enrichment Grant through Occidental College. Support for E.T. was provided, in part, by a postdoctoral fellowship from the German Research Foundation (DFG TI 973/1-1). Support for V.J.O. was provided, in part, by the Gordon and Betty Moore Foundation (grant no. 3780). The research was primarily supported by U.S. NSF grants OCE 1635219 (to E.E.C), OCE 1634172 (to L.A.L. and G.W.R.), and OCE 1634002 (to V.J.O.). Sample collection and export permits were acquired through the Costa Rican Ministry of the Environment and Energy (SINAC-CUSBSE-PI-R-032-2018 and Academic License SINAC-SE-064-2018). Author contributions: S.K.G. conducted DNA analysis, including 16S rRNA barcoding and fluorescent microscope analyses, analyzed experimental data, wrote the manuscript with input from coauthors, and participated in both expeditions. E.T. performed electron microscopy analyses and participated in AT42-03. A.K. performed Sentry data analysis and wrote the manuscript. K.S.D. designed and performed the incubation experiments, participated in both expeditions, and managed the SRA submission. S.W.M. designed and performed the incubation experiments and participated in both expeditions. F.W. performed fluorescent microscopy analyses. R.W.L. performed the isotope analyses. G.W.R. was a principal investigator on the NSF-funded project, fixed the specimens for study (including seamount worms), coordinated and interpreted the electron microscopy analyses, identified and is naming the worm species, and participated in all expeditions. L.A.L. was a principal investigator on the NSF-funded project, coordinated isotope analyses, wrote the manuscript, and participated in both expeditions. E.E.C. was a principal investigator on the NSF-funded project and chief scientist on both expeditions. V.J.O. was a principal investigator on the NSF-funded project, designed the incubation experiments, and participated in both expeditions. All authors contributed to data interpretation and editing of the paper. All authors declare that they have no competing interests. Data and materials availability: 16S rRNA sequences for bacterial isolates are available from GenBank under accession numbers MN416048 through MN416065. The raw Illumina 16S rRNA barcode sequences and metadata collected in this study are available from the Dryad Digital Repository (https://doi.org/10.5061/dryad.wdbrv15jq) and the NCBI Small Read Archive (BioProject no. PRJNA599018). Animal images and specimens were vouchered (Laminatubus catalog no. A9589 and Bispira catalog no.A9598) for long-term archiving into the Benthic Invertebrate Collection at Scripps Institution of Oceanography (https://sioapps.ucsd.edu/collections/bi/).
Funders:
Funding AgencyGrant Number
Occidental CollegeUNSPECIFIED
Deutsche Forschungsgemeinschaft (DFG)TI 973/1-1
Gordon and Betty Moore Foundation3780
NSFOCE-1635219
NSFOCE-1634172
NSFOCE-1634002
Subject Keywords:serpulid, sabellid, Serpulidae, Sabellidae, Annelida, methane seep, methanotrophy, symbiosis, deep-sea
Issue or Number:14
Record Number:CaltechAUTHORS:20200102-085056769
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20200102-085056769
Official Citation:Methanotrophic bacterial symbionts fuel dense populations of deep-sea feather duster worms (Sabellida, Annelida) and extend the spatial influence of methane seepage BY SHANA K. GOFFREDI, EKIN TILIC, SEAN W. MULLIN, KATHERINE S. DAWSON, ABIGAIL KELLER, RAYMOND W. LEE, FABAI WU, LISA A. LEVIN, GREG W. ROUSE, ERIK E. CORDES, VICTORIA J. ORPHAN Science Advances 03 Apr 2020: Vol. 6, no. 14, eaay8562. DOI: 10.1126/sciadv.aay8562
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:100444
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:02 Jan 2020 19:41
Last Modified:04 Apr 2020 03:51

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