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Title: Trichodesmium genome maintains abundant, widespread noncoding DNA in situ, despite oligotrophic lifestyle

Abstract

Understanding the evolution of the free-living, cyanobacterial, diazotroph Trichodesmium is of great importance due to its critical role in oceanic biogeochemistry and primary production. Unlike the other >150 available genomes of free-living cyanobacteria, only 63.8% of the Trichodesmium erythraeum (strain IMS101) genome is predicted to encode protein, which is 20-25% less than the average for other cyanobacteria and non-pathogenic, free-living bacteria. We use distinctive isolates and metagenomic data to show that low coding density observed in IMS101 is a common feature of the Trichodesmium genus both in culture and in situ. Transcriptome analysis indicates that 86% of the non-coding space is expressed, although the function of these transcripts is unclear. The density of noncoding, possible regulatory elements predicted in Trichodesmium, when normalized per intergenic kilobase, was comparable and two fold higher than that found in the gene dense genomes of the sympatric cyanobacterial genera Synechococcus and Prochlorococcus, respectively. Conserved Trichodesmium ncRNA secondary structures were predicted between most culture and metagenomic sequences lending support to the structural conservation. Conservation of these intergenic regions in spatiotemporally separated Trichodesmium populations suggests possible genus-wide selection for their maintenance. These large intergenic spacers may have developed during intervals of strong genetic drift caused by periodicmore » blooms of a subset of genotypes, which may have reduced effective population size. In conclusion, our data suggest that transposition of selfish DNA, low effective population size, and high fidelity replication allowed the unusual ‘inflation’ of noncoding sequence observed in Trichodesmium despite its oligotrophic lifestyle.« less

Authors:
; ; ; ; ; ; ; ; ; ; ; ; ; ;
Publication Date:
Research Org.:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States); USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
Contributing Org.:
Univ. of Southern California, Los Angeles, CA (United States); Woods Hole Oceanographic Inst., Woods Hole, MA (United States); Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
OSTI Identifier:
1208769
Alternate Identifier(s):
OSTI ID: 1286733
Report Number(s):
PNNL-SA-108623
Journal ID: ISSN 0027-8424; KP1601010
Grant/Contract Number:
AC05-76RL01830; AC02-05CH11231; AC03-76SF00098
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 112; Journal Issue: 14; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; genomics; cyanobacteria; marine biology; oligotrophic; evolution genomics; nitrogen fixation

Citation Formats

Walworth, Nathan, Pfreundt, Ulrike, Nelson, William C., Mincer, Tracy, Heidelberg, John F., Fu, Feixue, Waterbury, John B., Glavina del Rio, Tijana, Goodwin, Lynne, Kyrpides, Nikos C., Land, Miriam L., Woyke, Tanja, Hutchins, David A., Hess, Wolfgang R., and Webb, Eric A. Trichodesmium genome maintains abundant, widespread noncoding DNA in situ, despite oligotrophic lifestyle. United States: N. p., 2015. Web. doi:10.1073/pnas.1422332112.
Walworth, Nathan, Pfreundt, Ulrike, Nelson, William C., Mincer, Tracy, Heidelberg, John F., Fu, Feixue, Waterbury, John B., Glavina del Rio, Tijana, Goodwin, Lynne, Kyrpides, Nikos C., Land, Miriam L., Woyke, Tanja, Hutchins, David A., Hess, Wolfgang R., & Webb, Eric A. Trichodesmium genome maintains abundant, widespread noncoding DNA in situ, despite oligotrophic lifestyle. United States. doi:10.1073/pnas.1422332112.
Walworth, Nathan, Pfreundt, Ulrike, Nelson, William C., Mincer, Tracy, Heidelberg, John F., Fu, Feixue, Waterbury, John B., Glavina del Rio, Tijana, Goodwin, Lynne, Kyrpides, Nikos C., Land, Miriam L., Woyke, Tanja, Hutchins, David A., Hess, Wolfgang R., and Webb, Eric A. Mon . "Trichodesmium genome maintains abundant, widespread noncoding DNA in situ, despite oligotrophic lifestyle". United States. doi:10.1073/pnas.1422332112. https://www.osti.gov/servlets/purl/1208769.
@article{osti_1208769,
title = {Trichodesmium genome maintains abundant, widespread noncoding DNA in situ, despite oligotrophic lifestyle},
author = {Walworth, Nathan and Pfreundt, Ulrike and Nelson, William C. and Mincer, Tracy and Heidelberg, John F. and Fu, Feixue and Waterbury, John B. and Glavina del Rio, Tijana and Goodwin, Lynne and Kyrpides, Nikos C. and Land, Miriam L. and Woyke, Tanja and Hutchins, David A. and Hess, Wolfgang R. and Webb, Eric A.},
abstractNote = {Understanding the evolution of the free-living, cyanobacterial, diazotroph Trichodesmium is of great importance due to its critical role in oceanic biogeochemistry and primary production. Unlike the other >150 available genomes of free-living cyanobacteria, only 63.8% of the Trichodesmium erythraeum (strain IMS101) genome is predicted to encode protein, which is 20-25% less than the average for other cyanobacteria and non-pathogenic, free-living bacteria. We use distinctive isolates and metagenomic data to show that low coding density observed in IMS101 is a common feature of the Trichodesmium genus both in culture and in situ. Transcriptome analysis indicates that 86% of the non-coding space is expressed, although the function of these transcripts is unclear. The density of noncoding, possible regulatory elements predicted in Trichodesmium, when normalized per intergenic kilobase, was comparable and two fold higher than that found in the gene dense genomes of the sympatric cyanobacterial genera Synechococcus and Prochlorococcus, respectively. Conserved Trichodesmium ncRNA secondary structures were predicted between most culture and metagenomic sequences lending support to the structural conservation. Conservation of these intergenic regions in spatiotemporally separated Trichodesmium populations suggests possible genus-wide selection for their maintenance. These large intergenic spacers may have developed during intervals of strong genetic drift caused by periodic blooms of a subset of genotypes, which may have reduced effective population size. In conclusion, our data suggest that transposition of selfish DNA, low effective population size, and high fidelity replication allowed the unusual ‘inflation’ of noncoding sequence observed in Trichodesmium despite its oligotrophic lifestyle.},
doi = {10.1073/pnas.1422332112},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 14,
volume = 112,
place = {United States},
year = {Mon Mar 23 00:00:00 EDT 2015},
month = {Mon Mar 23 00:00:00 EDT 2015}
}

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