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Nitrate-based niche differentiation by distinct sulfate-reducing bacteria involved in the anaerobic oxidation of methane.
ISME J. 2014 Jan; 8(1):150-63.IJ

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 (15)N-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.

Authors+Show Affiliations

Division of Biology, California Institute of Technology, Pasadena, CA, USA.Division of Geological and Planetary Sciences, California Institute of Technology, Pasadena, CA, USA.Global Environmental Center, California Institute of Technology, Pasadena, CA, USA.Division of Geological and Planetary Sciences, California Institute of Technology, Pasadena, CA, USA.

Pub Type(s)

Journal Article
Research Support, U.S. Gov't, Non-P.H.S.

Language

eng

PubMed ID

24008326

Citation

Green-Saxena, A, et al. "Nitrate-based Niche Differentiation By Distinct Sulfate-reducing Bacteria Involved in the Anaerobic Oxidation of Methane." The ISME Journal, vol. 8, no. 1, 2014, pp. 150-63.
Green-Saxena A, Dekas AE, Dalleska NF, et al. Nitrate-based niche differentiation by distinct sulfate-reducing bacteria involved in the anaerobic oxidation of methane. ISME J. 2014;8(1):150-63.
Green-Saxena, A., Dekas, A. E., Dalleska, N. F., & Orphan, V. J. (2014). Nitrate-based niche differentiation by distinct sulfate-reducing bacteria involved in the anaerobic oxidation of methane. The ISME Journal, 8(1), 150-63. https://doi.org/10.1038/ismej.2013.147
Green-Saxena A, et al. Nitrate-based Niche Differentiation By Distinct Sulfate-reducing Bacteria Involved in the Anaerobic Oxidation of Methane. ISME J. 2014;8(1):150-63. PubMed PMID: 24008326.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Nitrate-based niche differentiation by distinct sulfate-reducing bacteria involved in the anaerobic oxidation of methane. AU - Green-Saxena,A, AU - Dekas,A E, AU - Dalleska,N F, AU - Orphan,V J, Y1 - 2013/09/05/ PY - 2013/03/12/received PY - 2013/07/19/revised PY - 2013/07/22/accepted PY - 2013/9/7/entrez PY - 2013/9/7/pubmed PY - 2014/2/12/medline SP - 150 EP - 63 JF - The ISME journal JO - ISME J VL - 8 IS - 1 N2 - 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 (15)N-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. SN - 1751-7370 UR - https://www.unboundmedicine.com/medline/citation/24008326/Nitrate_based_niche_differentiation_by_distinct_sulfate_reducing_bacteria_involved_in_the_anaerobic_oxidation_of_methane_ L2 - http://dx.doi.org/10.1038/ismej.2013.147 DB - PRIME DP - Unbound Medicine ER -