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

Abstract

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) indicatedmore » 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.« less

Authors:
 [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
Publication Date:
Research Org.:
Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States)
Sponsoring Org.:
USDOE; National Aeronautics and Space Administration (NASA)
OSTI Identifier:
1396225
Report Number(s):
LLNL-JRNL-652431
Journal ID: ISSN 1664-302X
Grant/Contract Number:  
AC52-07NA27344; SCW1039
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Volume: 5; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES; 59 BASIC BIOLOGICAL SCIENCES; 37 INORGANIC, ORGANIC, PHYSICAL AND ANALYTICAL CHEMISTRY; microbial mats; hydrogen; fermentation; Guerrero Negro; NanoSIMS

Citation Formats

Lee, Jackson Z., Burow, Luke C., Woebken, Dagmar, Everroad, R. Craig, Kubo, Mike D., Spormann, Alfred M., Weber, Peter K., Pett-Ridge, Jennifer, Bebout, Brad M., and Hoehler, Tori M. Fermentation couples Chloroflexi and sulfate-reducing bacteria to Cyanobacteria in hypersaline microbial mats. United States: N. p., 2014. Web. doi:10.3389/fmicb.2014.00061.
Lee, Jackson Z., Burow, Luke C., Woebken, Dagmar, Everroad, R. Craig, Kubo, Mike D., Spormann, Alfred M., Weber, Peter K., Pett-Ridge, Jennifer, Bebout, Brad M., & Hoehler, Tori M. Fermentation couples Chloroflexi and sulfate-reducing bacteria to Cyanobacteria in hypersaline microbial mats. United States. https://doi.org/10.3389/fmicb.2014.00061
Lee, Jackson Z., Burow, Luke C., Woebken, Dagmar, Everroad, R. Craig, Kubo, Mike D., Spormann, Alfred M., Weber, Peter K., Pett-Ridge, Jennifer, Bebout, Brad M., and Hoehler, Tori M. 2014. "Fermentation couples Chloroflexi and sulfate-reducing bacteria to Cyanobacteria in hypersaline microbial mats". United States. https://doi.org/10.3389/fmicb.2014.00061. https://www.osti.gov/servlets/purl/1396225.
@article{osti_1396225,
title = {Fermentation couples Chloroflexi and sulfate-reducing bacteria to Cyanobacteria in hypersaline microbial mats},
author = {Lee, Jackson Z. and Burow, Luke C. and Woebken, Dagmar and Everroad, R. Craig and Kubo, Mike D. and Spormann, Alfred M. and Weber, Peter K. and Pett-Ridge, Jennifer and Bebout, Brad M. and Hoehler, Tori M.},
abstractNote = {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.},
doi = {10.3389/fmicb.2014.00061},
url = {https://www.osti.gov/biblio/1396225}, journal = {Frontiers in Microbiology},
issn = {1664-302X},
number = ,
volume = 5,
place = {United States},
year = {Wed Jan 01 00:00:00 EST 2014},
month = {Wed Jan 01 00:00:00 EST 2014}
}

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Works referenced in this record:

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


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


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


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


Molecular characterization of sulfate-reducing bacteria in the Guaymas basin
text, January 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


Works referencing / citing this record:

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


Microsensor measurements of hydrogen gas dynamics in cyanobacterial microbial mats
journal, July 2015


Hydrogen Dynamics in Cyanobacteria Dominated Microbial Mats Measured by Novel Combined H2/H2S and H2/O2 Microsensors
journal, October 2017


Screening of polyhydroxyalkanoate-producing bacteria and PhaC-encoding genes in two hypersaline microbial mats from Guerrero Negro, Baja California Sur, Mexico
journal, January 2018