Evidence of a large novel gene pool associated with prokaryotic genomic islands.

Microbial genes that are "novel" (no detectable homologs in other species) have become of increasing interest as environmental sampling suggests that there are many more such novel genes in yet-to-be-cultured microorganisms. By analyzing known microbial genomic islands and prophages, we de...

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Main Authors: William W L Hsiao, Korine Ung, Dana Aeschliman, Jenny Bryan, B Brett Finlay, Fiona S L Brinkman
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2005-11-01
Series:PLoS Genetics
Online Access:http://europepmc.org/articles/PMC1285063?pdf=render
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spelling doaj-34b6b414523e44a48536e7f0b76055662020-11-24T21:44:32ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042005-11-0115e6210.1371/journal.pgen.0010062Evidence of a large novel gene pool associated with prokaryotic genomic islands.William W L HsiaoKorine UngDana AeschlimanJenny BryanB Brett FinlayFiona S L BrinkmanMicrobial genes that are "novel" (no detectable homologs in other species) have become of increasing interest as environmental sampling suggests that there are many more such novel genes in yet-to-be-cultured microorganisms. By analyzing known microbial genomic islands and prophages, we developed criteria for systematic identification of putative genomic islands (clusters of genes of probable horizontal origin in a prokaryotic genome) in 63 prokaryotic genomes, and then characterized the distribution of novel genes and other features. All but a few of the genomes examined contained significantly higher proportions of novel genes in their predicted genomic islands compared with the rest of their genome (Paired t test = 4.43E-14 to 1.27E-18, depending on method). Moreover, the reverse observation (i.e., higher proportions of novel genes outside of islands) never reached statistical significance in any organism examined. We show that this higher proportion of novel genes in predicted genomic islands is not due to less accurate gene prediction in genomic island regions, but likely reflects a genuine increase in novel genes in these regions for both bacteria and archaea. This represents the first comprehensive analysis of novel genes in prokaryotic genomic islands and provides clues regarding the origin of novel genes. Our collective results imply that there are different gene pools associated with recently horizontally transmitted genomic regions versus regions that are primarily vertically inherited. Moreover, there are more novel genes within the gene pool associated with genomic islands. Since genomic islands are frequently associated with a particular microbial adaptation, such as antibiotic resistance, pathogen virulence, or metal resistance, this suggests that microbes may have access to a larger "arsenal" of novel genes for adaptation than previously thought.http://europepmc.org/articles/PMC1285063?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author William W L Hsiao
Korine Ung
Dana Aeschliman
Jenny Bryan
B Brett Finlay
Fiona S L Brinkman
spellingShingle William W L Hsiao
Korine Ung
Dana Aeschliman
Jenny Bryan
B Brett Finlay
Fiona S L Brinkman
Evidence of a large novel gene pool associated with prokaryotic genomic islands.
PLoS Genetics
author_facet William W L Hsiao
Korine Ung
Dana Aeschliman
Jenny Bryan
B Brett Finlay
Fiona S L Brinkman
author_sort William W L Hsiao
title Evidence of a large novel gene pool associated with prokaryotic genomic islands.
title_short Evidence of a large novel gene pool associated with prokaryotic genomic islands.
title_full Evidence of a large novel gene pool associated with prokaryotic genomic islands.
title_fullStr Evidence of a large novel gene pool associated with prokaryotic genomic islands.
title_full_unstemmed Evidence of a large novel gene pool associated with prokaryotic genomic islands.
title_sort evidence of a large novel gene pool associated with prokaryotic genomic islands.
publisher Public Library of Science (PLoS)
series PLoS Genetics
issn 1553-7390
1553-7404
publishDate 2005-11-01
description Microbial genes that are "novel" (no detectable homologs in other species) have become of increasing interest as environmental sampling suggests that there are many more such novel genes in yet-to-be-cultured microorganisms. By analyzing known microbial genomic islands and prophages, we developed criteria for systematic identification of putative genomic islands (clusters of genes of probable horizontal origin in a prokaryotic genome) in 63 prokaryotic genomes, and then characterized the distribution of novel genes and other features. All but a few of the genomes examined contained significantly higher proportions of novel genes in their predicted genomic islands compared with the rest of their genome (Paired t test = 4.43E-14 to 1.27E-18, depending on method). Moreover, the reverse observation (i.e., higher proportions of novel genes outside of islands) never reached statistical significance in any organism examined. We show that this higher proportion of novel genes in predicted genomic islands is not due to less accurate gene prediction in genomic island regions, but likely reflects a genuine increase in novel genes in these regions for both bacteria and archaea. This represents the first comprehensive analysis of novel genes in prokaryotic genomic islands and provides clues regarding the origin of novel genes. Our collective results imply that there are different gene pools associated with recently horizontally transmitted genomic regions versus regions that are primarily vertically inherited. Moreover, there are more novel genes within the gene pool associated with genomic islands. Since genomic islands are frequently associated with a particular microbial adaptation, such as antibiotic resistance, pathogen virulence, or metal resistance, this suggests that microbes may have access to a larger "arsenal" of novel genes for adaptation than previously thought.
url http://europepmc.org/articles/PMC1285063?pdf=render
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