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Carbonate-hosted microbial communities are prolific and pervasive methane oxidizers at geologically diverse marine methane seep sites

Marlow, Jeffrey J. and Hoer, Daniel and Jungbluth, Sean P. and Reynard, Linda M. and Gartman, Amy and Chavez, Marko S. and El-Naggar, Mohamed Y. and Tuross, Noreen and Orphan, Victoria J. and Girguis, Peter R. (2021) Carbonate-hosted microbial communities are prolific and pervasive methane oxidizers at geologically diverse marine methane seep sites. Proceedings of the National Academy of Sciences, 118 (25). Art. No. e2006857118. ISSN 0027-8424. PMCID PMC8237665. doi:10.1073/pnas.2006857118. https://resolver.caltech.edu/CaltechAUTHORS:20210621-144751286

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Abstract

At marine methane seeps, vast quantities of methane move through the shallow subseafloor, where it is largely consumed by microbial communities. This process plays an important role in global methane dynamics, but we have yet to identify all of the methane sinks in the deep sea. Here, we conducted a continental-scale survey of seven geologically diverse seafloor seeps and found that carbonate rocks from all sites host methane-oxidizing microbial communities with substantial methanotrophic potential. In laboratory-based mesocosm incubations, chimney-like carbonates from the newly described Point Dume seep off the coast of Southern California exhibited the highest rates of anaerobic methane oxidation measured to date. After a thorough analysis of physicochemical, electrical, and biological factors, we attribute this substantial metabolic activity largely to higher cell density, mineral composition, kinetic parameters including an elevated V_(max), and the presence of specific microbial lineages. Our data also suggest that other features, such as electrical conductance, rock particle size, and microbial community alpha diversity, may influence a sample’s methanotrophic potential, but these factors did not demonstrate clear patterns with respect to methane oxidation rates. Based on the apparent pervasiveness within seep carbonates of microbial communities capable of performing anaerobic oxidation of methane, as well as the frequent occurrence of carbonates at seeps, we suggest that rock-hosted methanotrophy may be an important contributor to marine methane consumption.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1073/pnas.2006857118DOIArticle
https://www.pnas.org/content/suppl/2021/06/11/2006857118.DCSupplementalPublisherSupporting Information
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8237665PubMed CentralArticle
https://www.ncbi.nlm.nih.gov/bioproject/PRJNA648152Related ItemData
ORCID:
AuthorORCID
Marlow, Jeffrey J.0000-0003-2858-8806
Hoer, Daniel0000-0002-0644-760X
Jungbluth, Sean P.0000-0001-9265-8341
Reynard, Linda M.0000-0001-5732-1532
Gartman, Amy0000-0001-9307-3062
Tuross, Noreen0000-0002-3080-4005
Orphan, Victoria J.0000-0002-5374-6178
Girguis, Peter R.0000-0002-3599-8160
Additional Information:© 2021 the Author(s). Published by PNAS. This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND). Edited by Donald E. Canfield, University of Southern Denmark, Odense M, Denmark, and approved April 29, 2021 (received for review April 10, 2020). We thank Jenny Delaney, Dr. Aude Picard, Stephanie Connon, Stephanie Hillsgrove, Dr. Douglas Richardson, and Dr. Nicole Raineault for experimental and logistical assistance in the collection of samples and data presented here. We also thank the vehicle and vessel captains, crew, and science party members aboard the R/V Atlantis during legs AT 26-12-SVC (with the deep submergence vehicle Alvin), AT 36 (with the deep submergence vehicle Alvin and the autonomous underwater vehicle Sentry), and AT 37-06 (with DSV Alvin) and the E/V Nautilus during legs NA-073 and NA-084 (with the remotely operated vehicle Hercules). We thank the Schmidt Ocean Institute for supporting expedition FK181005, the crew of the R/V Falkor, and the pilots of the ROV SUBastian. We thank the Ocean Exploration Trust, who supported the initial expeditions to the Point Dume study site. Some analyses presented here were conducted at the Harvard University Center for Nanoscale Systems, a member of the National Nanotechnology Coordinated Infrastructure Network, which is supported by the NSF under NSF Electrical, Communications and Cyber Systems Award 1541959. We thank the Harvard Center for Biological Imaging for infrastructure and support. This work was supported by the NSF under Grants NSF-1542506 and NSF OCE-1635365 to P.R.G. Any opinions, findings, and conclusions or recommendations expressed in this material are those of the non-US Geological Survey (USGS) author(s) and do not necessarily reflect the views of the NSF. This journal article has been peer reviewed and approved for publication consistent with USGS Fundamental Science Practices (https://pubs.usgs.gov/circ/1367/). Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the US Government. This work was also supported by NASA under Grant No. NNX17AB31G to P.R.G., issued through the Planetary Science and Technology Through Analog Research program. Data Availability: DNA sequences data have been deposited in the NCBI (PRJNA648152). All other study data are included in the article and/or supporting information. Author contributions: J.J.M. and P.R.G. designed research; J.J.M. and D.H. performed research; D.H., S.P.J., L.M.R., A.G., M.S.C., M.Y.E.-N., and N.T. contributed new reagents/analytic tools; J.J.M., S.P.J., L.M.R., A.G., M.S.C., M.Y.E.-N., V.J.O., and P.R.G. analyzed data; and J.J.M. and P.R.G. wrote the paper with revisions and feedback from all authors. The authors declare no competing interest. This article is a PNAS Direct Submission. This article contains supporting information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.2006857118/-/DCSupplemental.
Funders:
Funding AgencyGrant Number
NSFECCS-1541959
NSFDEB-1542506
NSFOCE-1635365
NASANNX17AB31G
Issue or Number:25
PubMed Central ID:PMC8237665
DOI:10.1073/pnas.2006857118
Record Number:CaltechAUTHORS:20210621-144751286
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20210621-144751286
Official Citation:Carbonate-hosted microbial communities are prolific and pervasive methane oxidizers at geologically diverse marine methane seep sites. Jeffrey J. Marlow, Daniel Hoer, Sean P. Jungbluth, Linda M. Reynard, Amy Gartman, Marko S. Chavez, Mohamed Y. El-Naggar, Noreen Tuross, Victoria J. Orphan, Peter R. Girguis. Proceedings of the National Academy of Sciences Jun 2021, 118 (25) e2006857118; DOI: 10.1073/pnas.2006857118
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:109500
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:21 Jun 2021 20:18
Last Modified:08 Jul 2021 16:49

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