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

Journal Article · · Frontiers in Microbiology
 [1];  [2];  [2];  [3];  [4];  [5];  [6];  [6];  [3];  [3]
  1. NASA Ames Research Center (ARC), Moffett Field, Mountain View, CA (United States). Exobiology Branch; Bay Area Environmental Research Inst., Sonoma, CA (United States)
  2. NASA Ames Research Center (ARC), Moffett Field, Mountain View, CA (United States). Exobiology Branch; Stanford Univ., CA (United States). Dept. of Civil and Environmental Engineering, and Chemical Engineering
  3. NASA Ames Research Center (ARC), Moffett Field, Mountain View, CA (United States). Exobiology Branch
  4. NASA Ames Research Center (ARC), Moffett Field, Mountain View, CA (United States). Exobiology Branch; SETI Inst., Mountain View, CA (United States)
  5. Stanford Univ., CA (United States). Dept. of Civil and Environmental Engineering, and Chemical Engineering
  6. Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States). Chemical Sciences Division

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.

Research Organization:
Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States)
Sponsoring Organization:
USDOE; National Aeronautics and Space Administration (NASA)
Grant/Contract Number:
AC52-07NA27344; SCW1039
OSTI ID:
1396225
Report Number(s):
LLNL-JRNL-652431
Journal Information:
Frontiers in Microbiology, Vol. 5; ISSN 1664-302X
Publisher:
Frontiers Research FoundationCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 46 works
Citation information provided by
Web of Science

References (30)

Quantitative Determination of Monosaccharides in Glycoproteins by High-Performance Liquid Chromatography with Highly Sensitive Fluorescence Detection journal August 1994
Nonselective and Efficient Fluorescent Labeling of Glycans Using 2-Amino Benzamide and Anthranilic Acid journal September 1995
Phylogenetic Diversity and Distribution of Dissimilatory Sulfite Reductase Genes from Deep-Sea Sediment Cores journal May 2007
Herbicides of photosystem II book January 1992
Microbial diversity in polluted harbor sediments II: Sulfate-reducing bacterial community assessment using terminal restriction fragment length polymorphism and clone library of dsrAB gene journal February 2008
Comparison of diazotroph community structure in Lyngbya sp. and Microcoleus chthonoplastes dominated microbial mats from Guerrero Negro, Baja, Mexico journal March 2004
Occurrence, Classification, and Biological Function of Hydrogenases:  An Overview journal October 2007
The role of microbial mats in the production of reduced gases on the early Earth journal July 2001
Micron-scale mapping of sulfur cycling across the oxycline of a cyanobacterial mat: a paired nanoSIMS and CARD-FISH approach journal June 2008
Experimental factors affecting PCR-based estimates of microbial species richness and evenness journal January 2010
Hydrogen production in photosynthetic microbial mats in the Elkhorn Slough estuary, Monterey Bay journal October 2011
Identification of a novel cyanobacterial group as active diazotrophs in a coastal microbial mat using NanoSIMS analysis journal January 2012
Anoxic carbon flux in photosynthetic microbial mats as revealed by metatranscriptomics journal November 2012
R: A Language for Data Analysis and Graphics journal September 1996
Long-Term Manipulations of Intact Microbial Mat Communities in a Greenhouse Collaboratory: Simulating Earth's Present and Past Field Environments journal December 2002
The rapid generation of mutation data matrices from protein sequences journal January 1992
ProtTest: selection of best-fit models of protein evolution journal January 2005
Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences journal May 2006
Competition for inorganic carbon between oxygenic and anoxygenic phototrophs in a hypersaline microbial mat, Guerrero Negro, Mexico journal January 2013
Microbial diversity of benthic mats along a tidal desiccation gradient journal April 2005
Sulfate-reducing bacteria in marine sediment (Aarhus Bay, Denmark): abundance and diversity related to geochemical zonation journal May 2009
Diversity and Stratification of Archaea in a Hypersaline Microbial Mat journal December 2008
Quantifying Microbial Diversity: Morphotypes, 16S rRNA Genes, and Carotenoids of Oxygenic Phototrophs in Microbial Mats journal February 1999
Determination of Nitrogen-Fixing Phylotypes in Lyngbya sp. and Microcoleus chthonoplastes Cyanobacterial Mats from Guerrero Negro, Baja California, Mexico journal April 2004
Clustered Genes Related to Sulfate Respiration in Uncultured Prokaryotes Support the Theory of Their Concomitant Horizontal Transfer journal September 2005
Molecular characterization of sulfate-reducing bacteria in the Guaymas basin text January 2003
Biogeochemistry of Hypersaline Microbial Mats Illustrates the Dynamics of Modern Microbial Ecosystems and the Early Evolution of the Biosphere journal April 2003
Potential N2 fixation by sulfate-reducing bacteria in a marine intertidal microbial mat journal January 2002
Spectrophotometric Determination Of Hydrogen Sulfide In Natural Waters journal May 1969
Rapid, small-volume, flow injection analysis for SCO2, and NH4+ in marine and freshwaters journal July 1992

Cited By (12)

From the Cell to the Ecosystem: The Physiological Evolution of Symbiosis journal November 2015
Evidence for H 2 consumption by uncultured Desulfobacterales in coastal sediments: H 2 -consuming sulfate reducers in coastal sediments journal September 2017
In Situ Hydrogen Dynamics in a Hot Spring Microbial Mat during a Diel Cycle journal May 2016
Screening of polyhydroxyalkanoate-producing bacteria and PhaC-encoding genes in two hypersaline microbial mats from Guerrero Negro, Baja California Sur, Mexico journal January 2018
Cyanobacterial reuse of extracellular organic carbon in microbial mats journal October 2015
Organismal and spatial partitioning of energy and macronutrient transformations within a hypersaline mat journal March 2017
Metagenomic assembly of new (sub)polar Cyanobacteria and their associated microbiome from non-axenic cultures journal September 2018
Metagenomic analysis of intertidal hypersaline microbial mats from Elkhorn Slough, California, grown with and without molybdate journal November 2017
Prokaryotic diversity and biogeochemical characteristics of benthic microbial ecosystems at La Brava, a hypersaline lake at Salar de Atacama, Chile journal November 2017
Microsensor measurements of hydrogen gas dynamics in cyanobacterial microbial mats journal July 2015
Glycine Cleavage Powers Photoheterotrophic Growth of Chloroflexus aurantiacus in the Absence of H2 journal December 2015
Hydrogen Dynamics in Cyanobacteria Dominated Microbial Mats Measured by Novel Combined H2/H2S and H2/O2 Microsensors journal October 2017