Community transcriptomics reveals universal patterns of protein sequence conservation in natural microbial communities

Background Combined metagenomic and metatranscriptomic datasets make it possible to study the molecular evolution of diverse microbial species recovered from their native habitats. The link between gene expression level and sequence conservation was examined using shotgun pyrosequencing of microb...

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Main Authors: Stewart, Frank J., Sharma, Adrian, Bryant, Jessica A., Eppley, John Marmaduke, DeLong, Edward
Other Authors: Massachusetts Institute of Technology. Department of Civil and Environmental Engineering
Format: Article
Language:en_US
Published: BioMed Central Ltd. 2011
Online Access:http://hdl.handle.net/1721.1/65635
https://orcid.org/0000-0001-8958-4345
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author Stewart, Frank J.
Sharma, Adrian
Bryant, Jessica A.
Eppley, John Marmaduke
DeLong, Edward
author2 Massachusetts Institute of Technology. Department of Civil and Environmental Engineering
author_facet Massachusetts Institute of Technology. Department of Civil and Environmental Engineering
Stewart, Frank J.
Sharma, Adrian
Bryant, Jessica A.
Eppley, John Marmaduke
DeLong, Edward
author_sort Stewart, Frank J.
collection MIT
description Background Combined metagenomic and metatranscriptomic datasets make it possible to study the molecular evolution of diverse microbial species recovered from their native habitats. The link between gene expression level and sequence conservation was examined using shotgun pyrosequencing of microbial community DNA and RNA from diverse marine environments, and from forest soil. Results Across all samples, expressed genes with transcripts in the RNA sample were significantly more conserved than non-expressed gene sets relative to best matches in reference databases. This discrepancy, observed for many diverse individual genomes and across entire communities, coincided with a shift in amino acid usage between these gene fractions. Expressed genes trended toward GC-enriched amino acids, consistent with a hypothesis of higher levels of functional constraint in this gene pool. Highly expressed genes were significantly more likely to fall within an orthologous gene set shared between closely related taxa (core genes). However, non-core genes, when expressed above the level of detection, were, on average, significantly more highly expressed than core genes based on transcript abundance normalized to gene abundance. Finally, expressed genes showed broad similarities in function across samples, being relatively enriched in genes of energy metabolism and underrepresented by genes of cell growth. Conclusions These patterns support the hypothesis, predicated on studies of model organisms, that gene expression level is a primary correlate of evolutionary rate across diverse microbial taxa from natural environments. Despite their complexity, meta-omic datasets can reveal broad evolutionary patterns across taxonomically, functionally, and environmentally diverse communities.
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spelling mit-1721.1/656352022-09-30T19:08:07Z Community transcriptomics reveals universal patterns of protein sequence conservation in natural microbial communities Stewart, Frank J. Sharma, Adrian Bryant, Jessica A. Eppley, John Marmaduke DeLong, Edward Massachusetts Institute of Technology. Department of Civil and Environmental Engineering DeLong, Edward Sharma, Adrian Bryant, Jessica A. Eppley, John Marmaduke DeLong, Edward Background Combined metagenomic and metatranscriptomic datasets make it possible to study the molecular evolution of diverse microbial species recovered from their native habitats. The link between gene expression level and sequence conservation was examined using shotgun pyrosequencing of microbial community DNA and RNA from diverse marine environments, and from forest soil. Results Across all samples, expressed genes with transcripts in the RNA sample were significantly more conserved than non-expressed gene sets relative to best matches in reference databases. This discrepancy, observed for many diverse individual genomes and across entire communities, coincided with a shift in amino acid usage between these gene fractions. Expressed genes trended toward GC-enriched amino acids, consistent with a hypothesis of higher levels of functional constraint in this gene pool. Highly expressed genes were significantly more likely to fall within an orthologous gene set shared between closely related taxa (core genes). However, non-core genes, when expressed above the level of detection, were, on average, significantly more highly expressed than core genes based on transcript abundance normalized to gene abundance. Finally, expressed genes showed broad similarities in function across samples, being relatively enriched in genes of energy metabolism and underrepresented by genes of cell growth. Conclusions These patterns support the hypothesis, predicated on studies of model organisms, that gene expression level is a primary correlate of evolutionary rate across diverse microbial taxa from natural environments. Despite their complexity, meta-omic datasets can reveal broad evolutionary patterns across taxonomically, functionally, and environmentally diverse communities. Gordon and Betty Moore Foundation Agouron Institute National Science Foundation (U.S.) Center for Microbial Oceanography: Research and Education 2011-09-09T19:17:15Z 2011-09-09T19:17:15Z 2011-03 2011-02 Article http://purl.org/eprint/type/JournalArticle 1474-760X 1465-6914 1474-7596 http://hdl.handle.net/1721.1/65635 Stewart, Frank J et al. “Community transcriptomics reveals universal patterns of protein sequence conservation in natural microbial communities.” Genome Biology 12 (2011): R26. https://orcid.org/0000-0001-8958-4345 en_US http://dx.doi.org/10.1186/gb-2011-12-3-r26 Genome Biology Creative Commons Attribution http://creativecommons.org/licenses/by/2.0/ application/pdf BioMed Central Ltd. BMC
spellingShingle Stewart, Frank J.
Sharma, Adrian
Bryant, Jessica A.
Eppley, John Marmaduke
DeLong, Edward
Community transcriptomics reveals universal patterns of protein sequence conservation in natural microbial communities
title Community transcriptomics reveals universal patterns of protein sequence conservation in natural microbial communities
title_full Community transcriptomics reveals universal patterns of protein sequence conservation in natural microbial communities
title_fullStr Community transcriptomics reveals universal patterns of protein sequence conservation in natural microbial communities
title_full_unstemmed Community transcriptomics reveals universal patterns of protein sequence conservation in natural microbial communities
title_short Community transcriptomics reveals universal patterns of protein sequence conservation in natural microbial communities
title_sort community transcriptomics reveals universal patterns of protein sequence conservation in natural microbial communities
url http://hdl.handle.net/1721.1/65635
https://orcid.org/0000-0001-8958-4345
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