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Title: Evolution of the syntrophic interaction between Desulfovibrio vulgaris and Methanosarcina barkeri: involvement of an ancient horizontal gene transfer

Abstract

The sulfate reducing bacteria Desulfovibrio vulgaris and the methanogenic archaea Methanosarcina barkeri can grow syntrophically on lactate. In this study, three functionally unknown genes of D. vulgaris, DVU2103, DVU2104 and DVU2108, were found to be up-regulated 2-4 fold following the lifestyle shift from syntroph to sulfatereducer; moreover, none of these genes were regulated when D. vulgaris was grown alone in various pure culture conditions. These results suggest that these genes may play roles related to the lifestyle change of D. vulgaris from syntroph to sulfate reducer. This hypothesis is further supported by phylogenomic analyses showing that homologies of these genes were only narrowly present in several groups of bacteria, most of which are restricted to a syntrophic life-style, such as Pelobacter carbinolicus, Syntrophobacter fumaroxidans, Syntrophomonas wolfei and Syntrophus aciditrophicus. Phylogenetic analysis showed that the genes tended to be clustered with archaeal genera, and they were rooted on archaeal species in the phylogenetic trees, suggesting that they originated from an archaeal methanogen and were horizontally transferred to a common ancestor of delta- Proteobacteria, Clostridia and Thermotogae. While lost in most species during evolution, these genes appear to have been retained in bacteria capable of syntrophic relationships, probably due to their providingmore » a selective advantage. In addition, no significant bias in codon and amino acid usages was detected between these genes and the rest of the D. vulgaris genome, suggesting these gene transfers may have occurred early in the evolutionary history so that sufficient time has elapsed to allow an adaptation to the codon and amino acid usages of D. vulgaris. This report provides novel insights into the origin and evolution of bacterial genes involved in the syntrophic lifestyle.« less

Authors:
; ; ; ;
Publication Date:
Research Org.:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
898620
Report Number(s):
PNNL-SA-51609
TRN: US200706%%233
DOE Contract Number:  
AC05-76RL01830
Resource Type:
Journal Article
Resource Relation:
Journal Name: Biochemical and Biophysical Research Communications, 352(1):48-54
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; AMINO ACIDS; BACTERIA; CODONS; DESULFOVIBRIO; GENES; HYPOTHESIS; ORIGIN; SULFATE-REDUCING BACTERIA; SULFATES; TREES; Syntrophy; Horizontal gene transfer involved in microbial syntrophy

Citation Formats

Scholten, Johannes C., Culley, David E., Brockman, Fred J., Wu, Gang, and Zhang, Weiwen. Evolution of the syntrophic interaction between Desulfovibrio vulgaris and Methanosarcina barkeri: involvement of an ancient horizontal gene transfer. United States: N. p., 2007. Web. doi:10.1016/j.bbrc.2006.10.164.
Scholten, Johannes C., Culley, David E., Brockman, Fred J., Wu, Gang, & Zhang, Weiwen. Evolution of the syntrophic interaction between Desulfovibrio vulgaris and Methanosarcina barkeri: involvement of an ancient horizontal gene transfer. United States. doi:10.1016/j.bbrc.2006.10.164.
Scholten, Johannes C., Culley, David E., Brockman, Fred J., Wu, Gang, and Zhang, Weiwen. Fri . "Evolution of the syntrophic interaction between Desulfovibrio vulgaris and Methanosarcina barkeri: involvement of an ancient horizontal gene transfer". United States. doi:10.1016/j.bbrc.2006.10.164.
@article{osti_898620,
title = {Evolution of the syntrophic interaction between Desulfovibrio vulgaris and Methanosarcina barkeri: involvement of an ancient horizontal gene transfer},
author = {Scholten, Johannes C. and Culley, David E. and Brockman, Fred J. and Wu, Gang and Zhang, Weiwen},
abstractNote = {The sulfate reducing bacteria Desulfovibrio vulgaris and the methanogenic archaea Methanosarcina barkeri can grow syntrophically on lactate. In this study, three functionally unknown genes of D. vulgaris, DVU2103, DVU2104 and DVU2108, were found to be up-regulated 2-4 fold following the lifestyle shift from syntroph to sulfatereducer; moreover, none of these genes were regulated when D. vulgaris was grown alone in various pure culture conditions. These results suggest that these genes may play roles related to the lifestyle change of D. vulgaris from syntroph to sulfate reducer. This hypothesis is further supported by phylogenomic analyses showing that homologies of these genes were only narrowly present in several groups of bacteria, most of which are restricted to a syntrophic life-style, such as Pelobacter carbinolicus, Syntrophobacter fumaroxidans, Syntrophomonas wolfei and Syntrophus aciditrophicus. Phylogenetic analysis showed that the genes tended to be clustered with archaeal genera, and they were rooted on archaeal species in the phylogenetic trees, suggesting that they originated from an archaeal methanogen and were horizontally transferred to a common ancestor of delta- Proteobacteria, Clostridia and Thermotogae. While lost in most species during evolution, these genes appear to have been retained in bacteria capable of syntrophic relationships, probably due to their providing a selective advantage. In addition, no significant bias in codon and amino acid usages was detected between these genes and the rest of the D. vulgaris genome, suggesting these gene transfers may have occurred early in the evolutionary history so that sufficient time has elapsed to allow an adaptation to the codon and amino acid usages of D. vulgaris. This report provides novel insights into the origin and evolution of bacterial genes involved in the syntrophic lifestyle.},
doi = {10.1016/j.bbrc.2006.10.164},
journal = {Biochemical and Biophysical Research Communications, 352(1):48-54},
number = ,
volume = ,
place = {United States},
year = {Fri Jan 05 00:00:00 EST 2007},
month = {Fri Jan 05 00:00:00 EST 2007}
}