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Title: Metabolic Adaptations of Azospirillum brasilense to Oxygen Stress by Cell-to-Cell Clumping and Flocculation

Abstract

The ability of bacteria to monitor their metabolism and adjust their behavior accordingly is critical to maintain competitiveness in the environment. The motile microaerophilic bacteriumAzospirillum brasilensenavigates oxygen gradients by aerotaxis in order to locate low oxygen concentrations that can support metabolism. When cells are exposed to elevated levels of oxygen in their surroundings, motileA. brasilensecells implement an alternative response to aerotaxis and form transient clumps by cell-to-cell interactions. Clumping was suggested to represent a behavior protecting motile cells from transiently elevated levels of aeration. Using the proteomics of wild-type and mutant strains affected in the extent of their clumping abilities, we show that cell-to-cell clumping represents a metabolic scavenging strategy that likely prepares the cells for further metabolic stresses. Analysis of mutants affected in carbon or nitrogen metabolism confirmed this assumption. The metabolic changes experienced as clumping progresses prime cells for flocculation, a morphological and metabolic shift of cells triggered under elevated-aeration conditions and nitrogen limitation. The analysis of various mutants during clumping and flocculation characterized an ordered set of changes in cell envelope properties accompanying the metabolic changes. These data also identify clumping and early flocculation to be behaviors compatible with the expression of nitrogen fixation genes, despite themore » elevated-aeration conditions. Finally, cell-to-cell clumping may thus license diazotrophy to microaerophilicA. brasilensecells under elevated oxygen conditions and prime them for long-term survival via flocculation if metabolic stress persists.« less

Authors:
 [1];  [2];  [1];  [1];  [3];  [1];  [1];  [2];  [4]
  1. Univ. of Tennessee, Knoxville, TN (United States). Dept. of Biochemistry, Cellular and Molecular Biology
  2. Univ. of Tennessee, Knoxville, TN (United States). Genome Science and Technology Graduate Program; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Chemical Sciences Division
  3. Univ. of Tennessee, Knoxville, TN (United States). Genome Science and Technology Graduate Program
  4. Univ. of Tennessee, Knoxville, TN (United States). Dept. of Biochemistry, Cellular and Molecular Biology; Univ. of Tennessee, Knoxville, TN (United States). Genome Science and Technology Graduate Program
Publication Date:
Research Org.:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation (NSF)
OSTI Identifier:
1324041
Grant/Contract Number:  
AC05-00OR22725; MCB-0919819; MCB-1330344
Resource Type:
Accepted Manuscript
Journal Name:
Applied and Environmental Microbiology
Additional Journal Information:
Journal Volume: 81; Journal Issue: 24; Journal ID: ISSN 0099-2240
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; diazotroph; exopolysaccharides; motility; nitrogenase; nitrogen fixation

Citation Formats

Bible, Amber N., Khalsa-Moyers, Gurusahai K., Mukherjee, Tanmoy, Green, Calvin S., Mishra, Priyanka, Purcell, Alicia, Aksenova, Anastasia, Hurst, Gregory B., and Alexandre, Gladys. Metabolic Adaptations of Azospirillum brasilense to Oxygen Stress by Cell-to-Cell Clumping and Flocculation. United States: N. p., 2015. Web. doi:10.1128/AEM.02782-15.
Bible, Amber N., Khalsa-Moyers, Gurusahai K., Mukherjee, Tanmoy, Green, Calvin S., Mishra, Priyanka, Purcell, Alicia, Aksenova, Anastasia, Hurst, Gregory B., & Alexandre, Gladys. Metabolic Adaptations of Azospirillum brasilense to Oxygen Stress by Cell-to-Cell Clumping and Flocculation. United States. https://doi.org/10.1128/AEM.02782-15
Bible, Amber N., Khalsa-Moyers, Gurusahai K., Mukherjee, Tanmoy, Green, Calvin S., Mishra, Priyanka, Purcell, Alicia, Aksenova, Anastasia, Hurst, Gregory B., and Alexandre, Gladys. Fri . "Metabolic Adaptations of Azospirillum brasilense to Oxygen Stress by Cell-to-Cell Clumping and Flocculation". United States. https://doi.org/10.1128/AEM.02782-15. https://www.osti.gov/servlets/purl/1324041.
@article{osti_1324041,
title = {Metabolic Adaptations of Azospirillum brasilense to Oxygen Stress by Cell-to-Cell Clumping and Flocculation},
author = {Bible, Amber N. and Khalsa-Moyers, Gurusahai K. and Mukherjee, Tanmoy and Green, Calvin S. and Mishra, Priyanka and Purcell, Alicia and Aksenova, Anastasia and Hurst, Gregory B. and Alexandre, Gladys},
abstractNote = {The ability of bacteria to monitor their metabolism and adjust their behavior accordingly is critical to maintain competitiveness in the environment. The motile microaerophilic bacteriumAzospirillum brasilensenavigates oxygen gradients by aerotaxis in order to locate low oxygen concentrations that can support metabolism. When cells are exposed to elevated levels of oxygen in their surroundings, motileA. brasilensecells implement an alternative response to aerotaxis and form transient clumps by cell-to-cell interactions. Clumping was suggested to represent a behavior protecting motile cells from transiently elevated levels of aeration. Using the proteomics of wild-type and mutant strains affected in the extent of their clumping abilities, we show that cell-to-cell clumping represents a metabolic scavenging strategy that likely prepares the cells for further metabolic stresses. Analysis of mutants affected in carbon or nitrogen metabolism confirmed this assumption. The metabolic changes experienced as clumping progresses prime cells for flocculation, a morphological and metabolic shift of cells triggered under elevated-aeration conditions and nitrogen limitation. The analysis of various mutants during clumping and flocculation characterized an ordered set of changes in cell envelope properties accompanying the metabolic changes. These data also identify clumping and early flocculation to be behaviors compatible with the expression of nitrogen fixation genes, despite the elevated-aeration conditions. Finally, cell-to-cell clumping may thus license diazotrophy to microaerophilicA. brasilensecells under elevated oxygen conditions and prime them for long-term survival via flocculation if metabolic stress persists.},
doi = {10.1128/AEM.02782-15},
journal = {Applied and Environmental Microbiology},
number = 24,
volume = 81,
place = {United States},
year = {Fri Sep 25 00:00:00 EDT 2015},
month = {Fri Sep 25 00:00:00 EDT 2015}
}

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