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Nitrate-based niche differentiation by distinct sulfate-reducing bacteria involved in the anaerobic oxidation of methane

Green-Saxena, A. and Dekas, A. E. and Dalleska, N. F. and Orphan, V. J. (2014) Nitrate-based niche differentiation by distinct sulfate-reducing bacteria involved in the anaerobic oxidation of methane. ISME Journal, 8 (1). pp. 150-163. ISSN 1751-7362. PMCID PMC3869021. http://resolver.caltech.edu/CaltechAUTHORS:20140116-093516040

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Abstract

Diverse associations between methanotrophic archaea (ANME) and sulfate-reducing bacterial groups (SRB) often co-occur in marine methane seeps; however, the ecophysiology of these different symbiotic associations has not been examined. Here, we applied a combination of molecular, geochemical and Fluorescence in situ hybridization (FISH) coupled to nanoscale secondary ion mass spectrometry (FISH-NanoSIMS) analyses of in situ seep sediments and methane-amended sediment incubations from diverse locations (Eel River Basin, Hydrate Ridge and Costa Rican Margin seeps) to investigate the distribution and physiology of a newly identified subgroup of the Desulfobulbaceae (seepDBB) found in consortia with ANME-2c archaea, and compared these with the more commonly observed associations between the same ANME partner and the Desulfobacteraceae (DSS). FISH analyses revealed aggregates of seepDBB cells in association with ANME-2 from both environmental samples and laboratory incubations that are distinct in their structure relative to co-occurring ANME/DSS consortia. ANME/seepDBB aggregates were most abundant in shallow sediment depths below sulfide-oxidizing microbial mats. Depth profiles of ANME/seepDBB aggregate abundance revealed a positive correlation with elevated porewater nitrate relative to ANME/DSS aggregates in all seep sites examined. This relationship with nitrate was supported by sediment microcosm experiments, in which the abundance of ANME/seepDBB was greater in nitrate-amended incubations relative to the unamended control. FISH-NanoSIMS additionally revealed significantly higher 15N-nitrate incorporation levels in individual aggregates of ANME/seepDBB relative to ANME/DSS aggregates from the same incubation. These combined results suggest that nitrate is a geochemical effector of ANME/seepDBB aggregate distribution, and provides a unique niche for these consortia through their utilization of a greater range of nitrogen substrates than the ANME/DSS.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1038/ismej.2013.147DOIArticle
http://www.nature.com/ismej/journal/v8/n1/full/ismej2013147a.htmlPublisherArticle
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3869021/PubMed CentralArticle
ORCID:
AuthorORCID
Dalleska, N. F.0000-0002-2059-1587
Orphan, V. J.0000-0002-5374-6178
Additional Information:© 2014 International Society for Microbial Ecology. Received 12 March 2013; revised 19 July 2013; accepted 22 July 2013; published online 5 September 2013. We would like to thank Grayson Chadwick for his help with image analysis, Elizabeth Trembath-Reichert for contributing clone sequences, Ankur Saxena for figure design, Yunbin Guan NanoSIMS technical assistance and Joshua Steele for statistical analyses. We would like to also acknowledge Tsege Embaye for methane and sulfate measurements from AT 15–11 and the science party of cruises AT 15–11, AT 15–44, AT 15–68 and AT 18–10 and pilots of the DSRV Alvin and ROV Jason for their assistance with various aspects of this work. Funding for this work was provided by the Department of Energy Division of Biological Research (DE-SC0004949; to VJO), and a National Science Foundation Graduate Research Fellowship (to AG-S). The editing of this work by AD was partially performed under the auspices of the US Department of Energy by Lawrence Livermore National Laboratory under Contract DE-AC52-07NA27344. Samples were collected with funding from the National Science Foundation (BIO-OCE 0825791; to VJO).
Funders:
Funding AgencyGrant Number
Department of Energy (DOE)DE-SC0004949
NSF Graduate Research FellowshipUNSPECIFIED
NSFOCE-0825791
Department of Energy (DOE)DE-AC52-07NA27344
Subject Keywords:niche differentiation; nitrate assimilation; Desulfobulbaceae; methane seep; symbiosis
PubMed Central ID:PMC3869021
Record Number:CaltechAUTHORS:20140116-093516040
Persistent URL:http://resolver.caltech.edu/CaltechAUTHORS:20140116-093516040
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:43402
Collection:CaltechAUTHORS
Deposited By: Jason Perez
Deposited On:16 Jan 2014 19:28
Last Modified:21 Jul 2017 19:49

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