期刊名称：Proceedings of the National Academy of Sciences
印刷版ISSN：0027-8424
电子版ISSN：1091-6490
出版年度：2015
卷号：112
期号：14
页码：4251-4256
DOI：10.1073/pnas.1422332112
语种：English
出版社：The National Academy of Sciences of the United States of America
摘要：SignificanceThe free-living cyanobacterium Trichodesmium is a major source of new nitrogen and fixed carbon to the tropical and subtropical oceans, but despite its importance, we know little about the molecular mechanisms it uses to succeed in its oligotrophic habitat. Here we show that its gene-sparse genome is littered with large, conserved, expressed intergenic spaces, which is atypical for most known free-living prokaryotes. Paradoxically, although its genome is enriched in predicted transposases and repeat sequences, it exhibits conserved intragenus synteny and similar intergenic architecture relative to its sympatric, gene-dense relatives Prochlorococcus and Synechococcus. This observation demonstrates a successful alternative to the genomic streamlining strategy observed in other free-living oligotrophs such as Prochlorococcus or Pelagibacter. Understanding the evolution of the free-living, cyanobacterial, diazotroph Trichodesmium is of great importance because of 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 nonpathogenic, 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 noncoding 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 twofold higher than that found in the gene-dense genomes of the sympatric cyanobacterial genera Synechococcus and Prochlorococcus, respectively. Conserved Trichodesmium noncoding RNA 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. 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.
