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Title: Cyanobacterial reuse of extracellular organic carbon in microbial mats

Abstract

Cyanobacterial organic matter excretion is crucial to carbon cycling in many microbial communities, but the nature and bioavailability of this C depend on unknown physiological functions. Cyanobacteria-dominated hypersaline laminated mats are a useful model ecosystem for the study of C flow in complex communities, as they use photosynthesis to sustain a more or less closed system. Although such mats have a large C reservoir in the extracellular polymeric substances (EPSs), the production and degradation of organic carbon is not well defined. To identify extracellular processes in cyanobacterial mats, we examined mats collected from Elkhorn Slough (ES) at Monterey Bay, California, for glycosyl and protein composition of the EPS. We found a prevalence of simple glucose polysaccharides containing either α or β (1,4) linkages, indicating distinct sources of glucose with differing enzymatic accessibility. Using proteomics, we identified cyanobacterial extracellular enzymes, and also detected activities that indicate a capacity for EPS degradation. In a less complex system, we characterized the EPS of a cyanobacterial isolate from ES, ESFC-1, and found the extracellular composition of biofilms produced by this unicyanobacterial culture were similar to that of natural mats. By tracing isotopically labeled EPS into single cells of ESFC-1, we demonstrated rapid incorporation ofmore » extracellular-derived carbon. Taken together, these results indicate cyanobacteria reuse excess organic carbon, constituting a dynamic pool of extracellular resources in these mats.« less

Authors:
 [1];  [1];  [2];  [2];  [1];  [2];  [1];  [1]; ORCiD logo [1]
  1. Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States), Physical and Life Sciences Directorate
  2. NASA Ames Research Center (ARC), Moffett Field, Mountain View, CA (United States), Exobiology Branch
Publication Date:
Research Org.:
Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States); Univ. of Georgia, Athens, GA (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1623770
Grant/Contract Number:  
AC52-07NA27344; FG02-93ER20097
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
The ISME Journal
Additional Journal Information:
Journal Volume: 10; Journal Issue: 5; Journal ID: ISSN 1751-7362
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
Environmental Sciences & Ecology; Microbiology

Citation Formats

Stuart, Rhona K., Mayali, Xavier, Lee, Jackson Z., Craig Everroad, R., Hwang, Mona, Bebout, Brad M., Weber, Peter K., Pett-Ridge, Jennifer, and Thelen, Michael P. Cyanobacterial reuse of extracellular organic carbon in microbial mats. United States: N. p., 2015. Web. doi:10.1038/ismej.2015.180.
Stuart, Rhona K., Mayali, Xavier, Lee, Jackson Z., Craig Everroad, R., Hwang, Mona, Bebout, Brad M., Weber, Peter K., Pett-Ridge, Jennifer, & Thelen, Michael P. Cyanobacterial reuse of extracellular organic carbon in microbial mats. United States. https://doi.org/10.1038/ismej.2015.180
Stuart, Rhona K., Mayali, Xavier, Lee, Jackson Z., Craig Everroad, R., Hwang, Mona, Bebout, Brad M., Weber, Peter K., Pett-Ridge, Jennifer, and Thelen, Michael P. Fri . "Cyanobacterial reuse of extracellular organic carbon in microbial mats". United States. https://doi.org/10.1038/ismej.2015.180. https://www.osti.gov/servlets/purl/1623770.
@article{osti_1623770,
title = {Cyanobacterial reuse of extracellular organic carbon in microbial mats},
author = {Stuart, Rhona K. and Mayali, Xavier and Lee, Jackson Z. and Craig Everroad, R. and Hwang, Mona and Bebout, Brad M. and Weber, Peter K. and Pett-Ridge, Jennifer and Thelen, Michael P.},
abstractNote = {Cyanobacterial organic matter excretion is crucial to carbon cycling in many microbial communities, but the nature and bioavailability of this C depend on unknown physiological functions. Cyanobacteria-dominated hypersaline laminated mats are a useful model ecosystem for the study of C flow in complex communities, as they use photosynthesis to sustain a more or less closed system. Although such mats have a large C reservoir in the extracellular polymeric substances (EPSs), the production and degradation of organic carbon is not well defined. To identify extracellular processes in cyanobacterial mats, we examined mats collected from Elkhorn Slough (ES) at Monterey Bay, California, for glycosyl and protein composition of the EPS. We found a prevalence of simple glucose polysaccharides containing either α or β (1,4) linkages, indicating distinct sources of glucose with differing enzymatic accessibility. Using proteomics, we identified cyanobacterial extracellular enzymes, and also detected activities that indicate a capacity for EPS degradation. In a less complex system, we characterized the EPS of a cyanobacterial isolate from ES, ESFC-1, and found the extracellular composition of biofilms produced by this unicyanobacterial culture were similar to that of natural mats. By tracing isotopically labeled EPS into single cells of ESFC-1, we demonstrated rapid incorporation of extracellular-derived carbon. Taken together, these results indicate cyanobacteria reuse excess organic carbon, constituting a dynamic pool of extracellular resources in these mats.},
doi = {10.1038/ismej.2015.180},
url = {https://www.osti.gov/biblio/1623770}, journal = {The ISME Journal},
issn = {1751-7362},
number = 5,
volume = 10,
place = {United States},
year = {2015},
month = {10}
}

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Works referenced in this record:

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    Disentangling the drivers of functional complexity at the metagenomic level in Shark Bay microbial mat microbiomes
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    The ecological risks of hydrogen peroxide as a cyanocide: its effect on the community structure of bacterioplankton
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    Feathermoss and epiphytic Nostoc cooperate differently: expanding the spectrum of plant–cyanobacteria symbiosis
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    Linking soil biology and chemistry in biological soil crust using isolate exometabolomics
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