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Title: Phenotype fingerprinting suggests the involvement of single-genotype consortia in degradation of aromatic compounds by Rhodopseudomonas palustris

Abstract

Understanding of cellular processes involved in the anaerobic degradation of complex organic compounds by microorganisms is crucial for development of innovative biotechnologies for bioethanol production and for efficient degradation of toxic organic compounds. In natural environment the degradation is usually accomplished by syntrophic consortia comprised of different bacterial species. Here we show that the metabolically versatile phototrophic bacterium Rhodopseudomonas palustris may form its own syntrophic consortia, when it grows anaerobically on p-coumarate or benzoate as a sole carbon source. In the study we reveal the consortia from a comparison of large-scale measurements of mRNA and protein expressions under p-coumarate and benzoate degrading conditions using a novel computational approach referred as phenotype fingerprinting. In this approach marker genes for known R. palustris phenotypes are employed to calculate their expression from the gene and protein expressions in each studied condition. Subpopulations of the consortia are inferred from the expression of phenotypes and known metabolic modes of the R. palustris growth. We find that p-coumarate degrading condition leads to at least three R. palustris subpopulations utilizing p-coumarate, benzoate, and CO2 and H2. Benzoate degrading condition also produces at least three subpopulations utilizing benzoate, CO2 and H2, and N2 and formate. Communication among syntrophsmore » and inter-syntrophic dynamics in each consortium are indicated by up-regulation of transporters and genes involved in the curli formation and chemotaxis. The photoautotrphic subpopulation found in both consortia is characterized by activation of two cbb operons and the uptake hydrogenase system. A specificity of N2-fixing subpopulation in the benzoate degrading consortium is the preferential activation of the vanadium nitrogenase over the molybdenum nitrogenase. The N2-fixing subpopulation in the consortium is confirmed by consumption of dissolved nitrogen gas under the benzoate degrading conditions.« less

Authors:
 [1];  [1];  [1];  [1];  [2];  [1]
  1. ORNL
  2. {Bob} L [ORNL
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
964694
DOE Contract Number:  
DE-AC05-00OR22725
Resource Type:
Journal Article
Journal Name:
PLoS ONE
Additional Journal Information:
Journal Volume: 4; Journal Issue: 2
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; AROMATICS; CARBON SOURCES; COMMUNICATIONS; GENES; HYDROGENASES; MICROORGANISMS; MOLYBDENUM; NITROGEN; NITROGENASE; ORGANIC COMPOUNDS; PHENOTYPE; PRODUCTION; PROTEINS; RHODOPSEUDOMONAS; SPECIFICITY; VANADIUM

Citation Formats

Karpinets, Tatiana V, Pelletier, Dale A, Pan, Chongle, Uberbacher, Edward C, Hettich, Robert, and Samatova, Nagiza F. Phenotype fingerprinting suggests the involvement of single-genotype consortia in degradation of aromatic compounds by Rhodopseudomonas palustris. United States: N. p., 2009. Web. doi:10.1371/journal.pone.0004615.
Karpinets, Tatiana V, Pelletier, Dale A, Pan, Chongle, Uberbacher, Edward C, Hettich, Robert, & Samatova, Nagiza F. Phenotype fingerprinting suggests the involvement of single-genotype consortia in degradation of aromatic compounds by Rhodopseudomonas palustris. United States. doi:10.1371/journal.pone.0004615.
Karpinets, Tatiana V, Pelletier, Dale A, Pan, Chongle, Uberbacher, Edward C, Hettich, Robert, and Samatova, Nagiza F. Thu . "Phenotype fingerprinting suggests the involvement of single-genotype consortia in degradation of aromatic compounds by Rhodopseudomonas palustris". United States. doi:10.1371/journal.pone.0004615.
@article{osti_964694,
title = {Phenotype fingerprinting suggests the involvement of single-genotype consortia in degradation of aromatic compounds by Rhodopseudomonas palustris},
author = {Karpinets, Tatiana V and Pelletier, Dale A and Pan, Chongle and Uberbacher, Edward C and Hettich, Robert and Samatova, Nagiza F},
abstractNote = {Understanding of cellular processes involved in the anaerobic degradation of complex organic compounds by microorganisms is crucial for development of innovative biotechnologies for bioethanol production and for efficient degradation of toxic organic compounds. In natural environment the degradation is usually accomplished by syntrophic consortia comprised of different bacterial species. Here we show that the metabolically versatile phototrophic bacterium Rhodopseudomonas palustris may form its own syntrophic consortia, when it grows anaerobically on p-coumarate or benzoate as a sole carbon source. In the study we reveal the consortia from a comparison of large-scale measurements of mRNA and protein expressions under p-coumarate and benzoate degrading conditions using a novel computational approach referred as phenotype fingerprinting. In this approach marker genes for known R. palustris phenotypes are employed to calculate their expression from the gene and protein expressions in each studied condition. Subpopulations of the consortia are inferred from the expression of phenotypes and known metabolic modes of the R. palustris growth. We find that p-coumarate degrading condition leads to at least three R. palustris subpopulations utilizing p-coumarate, benzoate, and CO2 and H2. Benzoate degrading condition also produces at least three subpopulations utilizing benzoate, CO2 and H2, and N2 and formate. Communication among syntrophs and inter-syntrophic dynamics in each consortium are indicated by up-regulation of transporters and genes involved in the curli formation and chemotaxis. The photoautotrphic subpopulation found in both consortia is characterized by activation of two cbb operons and the uptake hydrogenase system. A specificity of N2-fixing subpopulation in the benzoate degrading consortium is the preferential activation of the vanadium nitrogenase over the molybdenum nitrogenase. The N2-fixing subpopulation in the consortium is confirmed by consumption of dissolved nitrogen gas under the benzoate degrading conditions.},
doi = {10.1371/journal.pone.0004615},
journal = {PLoS ONE},
number = 2,
volume = 4,
place = {United States},
year = {2009},
month = {1}
}