Activity and interactions of methane seep microorganisms assessed by parallel transcription and FISH-NanoSIMS analyses

Dekas, Anne E.; Connon, Stephanie A.; Chadwick, Grayson L.; Trembath-Reichert, Elizabeth; Orphan, Victoria J.

doi:10.1038/ismej.2015.145

Title: Activity and interactions of methane seep microorganisms assessed by parallel transcription and FISH-NanoSIMS analyses

Journal Article · Tue Sep 22 00:00:00 EDT 2015 · The ISME Journal

DOI:https://doi.org/10.1038/ismej.2015.145· OSTI ID:1435726

Dekas, Anne E. ^[1]; Connon, Stephanie A. ^[1]; Chadwick, Grayson L. ^[1]; Trembath-Reichert, Elizabeth ^[1]; Orphan, Victoria J. ^[1]

California Inst. of Technology (CalTech), Pasadena, CA (United States). Division of Geological and Planetary Sciences

To characterize the activity and interactions of methanotrophic archaea (ANME) and Deltaproteo-bacteria at a methane-seeping mud volcano, we used two complimentary measures of microbial activity: a community-level analysis of the transcription of four genes (16S rRNA, methyl coenzyme M reductase A (mcrA), adenosine-5'-phosphosulfate reductase α-subunit (aprA), dinitrogenase reductase (nifH)), and a single-cell-level analysis of anabolic activity using fluorescence in situ hybridization coupled to nanoscale secondary ion mass spectrometry (FISH-NanoSIMS). Transcript analysis revealed that members of the deltaproteobacterial groups Desulfosarcina/Desulfococcus (DSS) and Desulfobulbaceae (DSB) exhibit increased rRNA expression in incubations with methane, suggestive of ANME-coupled activity. Direct analysis of anabolic activity in DSS cells in consortia with ANME by FISH-NanoSIMS confirmed their dependence on methanotrophy, with no ¹⁵NH$$+\atop{4}$$ assimilation detected without methane. In contrast, DSS and DSB cells found physically independent of ANME (i.e., single cells) were anabolically active in incubations both with and without methane. These single cells therefore comprise an active ‘free-living’ population, and are not dependent on methane or ANME activity. We investigated the possibility of N₂ fixation by seep Deltaproteobacteria and detected nifH transcripts closely related to those of cultured diazotrophic Deltaproteobacteria. However, nifH expression was methane-dependent. ¹⁵N₂ incorporation was not observed in single DSS cells, but was detected in single DSB cells. Interestingly, ¹⁵N₂ incorporation in single DSB cells was methane-dependent, raising the possibility that DSB cells acquired reduced ¹⁵N products from diazotrophic ANME while spatially coupled, and then subsequently dissociated. In conclusion, with this combined data set we address several outstanding questions in methane seep microbial ecosystems and highlight the benefit of measuring microbial activity in the context of spatial associations.

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Research Organization:: California Institute of Technology (CalTech), Pasadena, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: SC0003940; SC0004949; AC52-07NA27344

OSTI ID:: 1435726

Journal Information:: The ISME Journal, Vol. 10, Issue 3; ISSN 1751-7362

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 41 works

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