This article is part of the Research Topic Systems biology and ecology of microbial mat communities

Original Research ARTICLE

Front. Microbiol., 26 February 2014 | doi: 10.3389/fmicb.2014.00061

Fermentation couples Chloroflexi and sulfate-reducing bacteria to Cyanobacteria in hypersaline microbial mats

  • 1Exobiology Branch, NASA Ames Research Center, Moffett Field, CA, USA
  • 2Bay Area Environmental Research Institute, Sonoma, CA, USA
  • 3Departments of Civil and Environmental Engineering, and Chemical Engineering, Stanford University, Stanford, CA, USA
  • 4The SETI Institute, Mountain View, CA, USA
  • 5Lawrence Livermore National Lab, Chemical Sciences Division, Livermore, CA, USA

Past studies of hydrogen cycling in hypersaline microbial mats have shown an active nighttime cycle, with production largely from Cyanobacteria and consumption from sulfate-reducing bacteria (SRB). However, the mechanisms and magnitude of hydrogen cycling have not been extensively studied. Two mats types near Guerrero Negro, Mexico—permanently submerged Microcoleus microbial mat (GN-S), and intertidal Lyngbya microbial mat (GN-I)—were used in microcosm diel manipulation experiments with 3-(3,4-dichlorophenyl)-1,1-dimethylurea (DCMU), molybdate, ammonium addition, and physical disruption to understand the processes responsible for hydrogen cycling between mat microbes. Across microcosms, H2 production occurred under dark anoxic conditions with simultaneous production of a suite of organic acids. H2 production was not significantly affected by inhibition of nitrogen fixation, but rather appears to result from constitutive fermentation of photosynthetic storage products by oxygenic phototrophs. Comparison to accumulated glycogen and to CO2 flux indicated that, in the GN-I mat, fermentation released almost all of the carbon fixed via photosynthesis during the preceding day, primarily as organic acids. Across mats, although oxygenic and anoxygenic phototrophs were detected, cyanobacterial [NiFe]-hydrogenase transcripts predominated. Molybdate inhibition experiments indicated that SRBs from a wide distribution of DsrA phylotypes were responsible for H2 consumption. Incubation with 13C-acetate and NanoSIMS (secondary ion mass-spectrometry) indicated higher uptake in both Chloroflexi and SRBs relative to other filamentous bacteria. These manipulations and diel incubations confirm that Cyanobacteria were the main fermenters in Guerrero Negro mats and that the net flux of nighttime fermentation byproducts (not only hydrogen) was largely regulated by the interplay between Cyanobacteria, SRBs, and Chloroflexi.

Keywords: microbial mats, hydrogen, fermentation, Guerrero Negro, NanoSIMS

Citation: Lee JZ, Burow LC, Woebken D, Everroad RC, Kubo MD, Spormann AM Weber PK, Pett-Ridge J, Bebout BM and Hoehler TM (2014) Fermentation couples Chloroflexi and sulfate-reducing bacteria to Cyanobacteria in hypersaline microbial mats. Front. Microbiol. 5:61. doi: 10.3389/fmicb.2014.00061

Received: 28 November 2013; Paper pending published: 23 December 2013;
Accepted: 30 January 2014; Published online: 26 February 2014.

Edited by:

Donald A. Bryant, The Pennsylvania State University, USA

Reviewed by:

Niels-Ulrik Frigaard, University of Copenhagen, Denmark
John R. Spear, Colorado School of Mines, USA

Copyright © 2014 Lee, Burow, Woebken, Everroad, Kubo, Spormann, Weber, Pett-Ridge, Bebout and Hoehler. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

*Correspondence: Jackson Z. Lee, NASA Ames Research Center, PO Box 1, MS 239-4, Moffett Field, CA 94035, USA e-mail: jackson.z.lee@nasa.gov

Present address: Dagmar Woebken, Division of Microbial Ecology, Department of Microbiology and Ecosystem Science, University of Vienna, Vienna, Austria

Back to top