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Complete genome of streamlined marine actinobacterium Pontimonas salivibrio strain CL-TW6(T) adapted to coastal planktonic lifestyle

BACKGROUND: Pontimonas salivibrio strain CL-TW6(T) (=KCCM 90105 = JCM18206) was characterized as the type strain of a new genus within the Actinobacterial family Microbacteriaceae. It was isolated from a coastal marine environment in which members of Microbactericeae have not been previously charact...

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Autores principales: Cho, Byung Cheol, Hardies, Stephen C., Jang, Gwang Il, Hwang, Chung Yeon
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6106888/
https://www.ncbi.nlm.nih.gov/pubmed/30134835
http://dx.doi.org/10.1186/s12864-018-5019-9
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author Cho, Byung Cheol
Hardies, Stephen C.
Jang, Gwang Il
Hwang, Chung Yeon
author_facet Cho, Byung Cheol
Hardies, Stephen C.
Jang, Gwang Il
Hwang, Chung Yeon
author_sort Cho, Byung Cheol
collection PubMed
description BACKGROUND: Pontimonas salivibrio strain CL-TW6(T) (=KCCM 90105 = JCM18206) was characterized as the type strain of a new genus within the Actinobacterial family Microbacteriaceae. It was isolated from a coastal marine environment in which members of Microbactericeae have not been previously characterized. RESULTS: The genome of P. salivibrio CL-TW6(T) was a single chromosome of 1,760,810 bp. Genomes of this small size are typically found in bacteria growing slowly in oligotrophic zones and said to be streamlined. Phylogenetic analysis showed it to represent a lineage originating in the Microbacteriaceae radiation occurring before the snowball Earth glaciations, and to have a closer relationship with some streamlined bacteria known through metagenomic data. Several genomic characteristics typical of streamlined bacteria are found: %G + C is lower than non-streamlined members of the phylum; there are a minimal number of rRNA and tRNA genes, fewer paralogs in most gene families, and only two sigma factors; there is a noticeable absence of some nonessential metabolic pathways, including polyketide synthesis and catabolism of some amino acids. There was no indication of any phage genes or plasmids, however, a system of active insertion elements was present. P. salivibrio appears to be unusual in having polyrhamnose-based cell wall oligosaccharides instead of mycolic acid or teichoic acid-based oligosaccharides. Oddly, it conducts sulfate assimilation apparently for sulfating cell wall components, but not for synthesizing amino acids. One gene family it has more of, rather than fewer of, are toxin/antitoxin systems, which are thought to down-regulate growth during nutrient deprivation or other stressful conditions. CONCLUSIONS: Because of the relatively small number of paralogs and its relationship to the heavily characterized Mycobacterium tuberculosis, we were able to heavily annotate the genome of P. salivibrio CL-TW6(T). Its streamlined status and relationship to streamlined metagenomic constructs makes it an important reference genome for study of the streamlining concept. The final evolutionary trajectory of CL-TW6 (T) was to adapt to growth in a non-oligotrophic coastal zone. To understand that adaptive process, we give a thorough accounting of gene content, contrasting with both oligotrophic streamlined bacteria and large genome bacteria, and distinguishing between genes derived by vertical and horizontal descent. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-018-5019-9) contains supplementary material, which is available to authorized users.
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spelling pubmed-61068882018-08-29 Complete genome of streamlined marine actinobacterium Pontimonas salivibrio strain CL-TW6(T) adapted to coastal planktonic lifestyle Cho, Byung Cheol Hardies, Stephen C. Jang, Gwang Il Hwang, Chung Yeon BMC Genomics Research Article BACKGROUND: Pontimonas salivibrio strain CL-TW6(T) (=KCCM 90105 = JCM18206) was characterized as the type strain of a new genus within the Actinobacterial family Microbacteriaceae. It was isolated from a coastal marine environment in which members of Microbactericeae have not been previously characterized. RESULTS: The genome of P. salivibrio CL-TW6(T) was a single chromosome of 1,760,810 bp. Genomes of this small size are typically found in bacteria growing slowly in oligotrophic zones and said to be streamlined. Phylogenetic analysis showed it to represent a lineage originating in the Microbacteriaceae radiation occurring before the snowball Earth glaciations, and to have a closer relationship with some streamlined bacteria known through metagenomic data. Several genomic characteristics typical of streamlined bacteria are found: %G + C is lower than non-streamlined members of the phylum; there are a minimal number of rRNA and tRNA genes, fewer paralogs in most gene families, and only two sigma factors; there is a noticeable absence of some nonessential metabolic pathways, including polyketide synthesis and catabolism of some amino acids. There was no indication of any phage genes or plasmids, however, a system of active insertion elements was present. P. salivibrio appears to be unusual in having polyrhamnose-based cell wall oligosaccharides instead of mycolic acid or teichoic acid-based oligosaccharides. Oddly, it conducts sulfate assimilation apparently for sulfating cell wall components, but not for synthesizing amino acids. One gene family it has more of, rather than fewer of, are toxin/antitoxin systems, which are thought to down-regulate growth during nutrient deprivation or other stressful conditions. CONCLUSIONS: Because of the relatively small number of paralogs and its relationship to the heavily characterized Mycobacterium tuberculosis, we were able to heavily annotate the genome of P. salivibrio CL-TW6(T). Its streamlined status and relationship to streamlined metagenomic constructs makes it an important reference genome for study of the streamlining concept. The final evolutionary trajectory of CL-TW6 (T) was to adapt to growth in a non-oligotrophic coastal zone. To understand that adaptive process, we give a thorough accounting of gene content, contrasting with both oligotrophic streamlined bacteria and large genome bacteria, and distinguishing between genes derived by vertical and horizontal descent. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-018-5019-9) contains supplementary material, which is available to authorized users. BioMed Central 2018-08-22 /pmc/articles/PMC6106888/ /pubmed/30134835 http://dx.doi.org/10.1186/s12864-018-5019-9 Text en © The Author(s). 2018 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Cho, Byung Cheol
Hardies, Stephen C.
Jang, Gwang Il
Hwang, Chung Yeon
Complete genome of streamlined marine actinobacterium Pontimonas salivibrio strain CL-TW6(T) adapted to coastal planktonic lifestyle
title Complete genome of streamlined marine actinobacterium Pontimonas salivibrio strain CL-TW6(T) adapted to coastal planktonic lifestyle
title_full Complete genome of streamlined marine actinobacterium Pontimonas salivibrio strain CL-TW6(T) adapted to coastal planktonic lifestyle
title_fullStr Complete genome of streamlined marine actinobacterium Pontimonas salivibrio strain CL-TW6(T) adapted to coastal planktonic lifestyle
title_full_unstemmed Complete genome of streamlined marine actinobacterium Pontimonas salivibrio strain CL-TW6(T) adapted to coastal planktonic lifestyle
title_short Complete genome of streamlined marine actinobacterium Pontimonas salivibrio strain CL-TW6(T) adapted to coastal planktonic lifestyle
title_sort complete genome of streamlined marine actinobacterium pontimonas salivibrio strain cl-tw6(t) adapted to coastal planktonic lifestyle
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6106888/
https://www.ncbi.nlm.nih.gov/pubmed/30134835
http://dx.doi.org/10.1186/s12864-018-5019-9
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