Characterization of the First Cultured Psychrotolerant Representative of Legionella from Antarctica Reveals Its Unique Genome Structure
ABSTRACT Culture-independent analysis shows that Legionella spp. inhabit a wide range of low-temperature environments, but to date, no psychrotolerant or psychrophilic strains have been reported. Here, we characterized the first cultivated psychrotolerant representative, designated strain TUM19329T,...
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American Society for Microbiology
2021
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ftdoajarticles:oai:doaj.org/article:4796c8adcfe74c85863e14d173d55741 2023-05-15T13:36:56+02:00 Characterization of the First Cultured Psychrotolerant Representative of Legionella from Antarctica Reveals Its Unique Genome Structure Sho Shimada Ryosuke Nakai Kotaro Aoki Sakae Kudoh Satoshi Imura Norifumi Shimoeda Giichiro Ohno Kentaro Watanabe Yasunari Miyazaki Yoshikazu Ishii Kazuhiro Tateda 2021-10-01T00:00:00Z https://doi.org/10.1128/Spectrum.00424-21 https://doaj.org/article/4796c8adcfe74c85863e14d173d55741 EN eng American Society for Microbiology https://journals.asm.org/doi/10.1128/Spectrum.00424-21 https://doaj.org/toc/2165-0497 doi:10.1128/Spectrum.00424-21 2165-0497 https://doaj.org/article/4796c8adcfe74c85863e14d173d55741 Microbiology Spectrum, Vol 9, Iss 2 (2021) Legionella psychrotolerant insertion sequence horizontal gene transfer comparative genomic analysis cellular fatty acids Microbiology QR1-502 article 2021 ftdoajarticles https://doi.org/10.1128/Spectrum.00424-21 2022-12-31T10:39:40Z ABSTRACT Culture-independent analysis shows that Legionella spp. inhabit a wide range of low-temperature environments, but to date, no psychrotolerant or psychrophilic strains have been reported. Here, we characterized the first cultivated psychrotolerant representative, designated strain TUM19329T, isolated from an Antarctic lake using a polyphasic approach and comparative genomic analysis. A genome-wide phylogenetic tree indicated that this strain was phylogenetically separate at the species level. Strain TUM19329T shared common physiological traits (e.g., Gram-negative, limited growth on buffered charcoal-yeast extract α-ketoglutarate [BCYEα] agar with l-cysteine requirements) with its relatives, but it also showed psychrotolerant growth properties (e.g., growth at 4°C to 25°C). Moreover, this strain altered its own cellular fatty acid composition to accumulate unsaturated fatty acid at a lower temperature, which may help maintain the cell membrane fluidity. Through comparative genomic analysis, we found that this strain possessed massive mobile genetic elements compared with other species, amounting to up to 17% of the total genes. The majority of the elements were the result of the spread of only a few insertion sequences (ISs), which were spread throughout the genome by a “copy-and-paste” mechanism. Furthermore, we found metabolic genes, such as fatty acid synthesis-related genes, acquired by horizontal gene transfer (HGT). The expansion of ISs and HGT events may play a major role in shaping the phenotype and physiology of this strain. On the basis of the features presented here, we propose a new species—Legionella antarctica sp. nov.—represented by strain TUM19329T (= GTC 22699T = NCTC 14581T). IMPORTANCE This study characterized a unique cultivated representative of the genus Legionella isolated from an Antarctic lake. This psychrotolerant strain had some common properties of known Legionella species but also displayed other characteristics, such as plasticity in fatty acid composition and an enrichment ... Article in Journal/Newspaper Antarc* Antarctic Antarctica Directory of Open Access Journals: DOAJ Articles Antarctic Microbiology Spectrum 9 2 |
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Open Polar |
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Directory of Open Access Journals: DOAJ Articles |
op_collection_id |
ftdoajarticles |
language |
English |
topic |
Legionella psychrotolerant insertion sequence horizontal gene transfer comparative genomic analysis cellular fatty acids Microbiology QR1-502 |
spellingShingle |
Legionella psychrotolerant insertion sequence horizontal gene transfer comparative genomic analysis cellular fatty acids Microbiology QR1-502 Sho Shimada Ryosuke Nakai Kotaro Aoki Sakae Kudoh Satoshi Imura Norifumi Shimoeda Giichiro Ohno Kentaro Watanabe Yasunari Miyazaki Yoshikazu Ishii Kazuhiro Tateda Characterization of the First Cultured Psychrotolerant Representative of Legionella from Antarctica Reveals Its Unique Genome Structure |
topic_facet |
Legionella psychrotolerant insertion sequence horizontal gene transfer comparative genomic analysis cellular fatty acids Microbiology QR1-502 |
description |
ABSTRACT Culture-independent analysis shows that Legionella spp. inhabit a wide range of low-temperature environments, but to date, no psychrotolerant or psychrophilic strains have been reported. Here, we characterized the first cultivated psychrotolerant representative, designated strain TUM19329T, isolated from an Antarctic lake using a polyphasic approach and comparative genomic analysis. A genome-wide phylogenetic tree indicated that this strain was phylogenetically separate at the species level. Strain TUM19329T shared common physiological traits (e.g., Gram-negative, limited growth on buffered charcoal-yeast extract α-ketoglutarate [BCYEα] agar with l-cysteine requirements) with its relatives, but it also showed psychrotolerant growth properties (e.g., growth at 4°C to 25°C). Moreover, this strain altered its own cellular fatty acid composition to accumulate unsaturated fatty acid at a lower temperature, which may help maintain the cell membrane fluidity. Through comparative genomic analysis, we found that this strain possessed massive mobile genetic elements compared with other species, amounting to up to 17% of the total genes. The majority of the elements were the result of the spread of only a few insertion sequences (ISs), which were spread throughout the genome by a “copy-and-paste” mechanism. Furthermore, we found metabolic genes, such as fatty acid synthesis-related genes, acquired by horizontal gene transfer (HGT). The expansion of ISs and HGT events may play a major role in shaping the phenotype and physiology of this strain. On the basis of the features presented here, we propose a new species—Legionella antarctica sp. nov.—represented by strain TUM19329T (= GTC 22699T = NCTC 14581T). IMPORTANCE This study characterized a unique cultivated representative of the genus Legionella isolated from an Antarctic lake. This psychrotolerant strain had some common properties of known Legionella species but also displayed other characteristics, such as plasticity in fatty acid composition and an enrichment ... |
format |
Article in Journal/Newspaper |
author |
Sho Shimada Ryosuke Nakai Kotaro Aoki Sakae Kudoh Satoshi Imura Norifumi Shimoeda Giichiro Ohno Kentaro Watanabe Yasunari Miyazaki Yoshikazu Ishii Kazuhiro Tateda |
author_facet |
Sho Shimada Ryosuke Nakai Kotaro Aoki Sakae Kudoh Satoshi Imura Norifumi Shimoeda Giichiro Ohno Kentaro Watanabe Yasunari Miyazaki Yoshikazu Ishii Kazuhiro Tateda |
author_sort |
Sho Shimada |
title |
Characterization of the First Cultured Psychrotolerant Representative of Legionella from Antarctica Reveals Its Unique Genome Structure |
title_short |
Characterization of the First Cultured Psychrotolerant Representative of Legionella from Antarctica Reveals Its Unique Genome Structure |
title_full |
Characterization of the First Cultured Psychrotolerant Representative of Legionella from Antarctica Reveals Its Unique Genome Structure |
title_fullStr |
Characterization of the First Cultured Psychrotolerant Representative of Legionella from Antarctica Reveals Its Unique Genome Structure |
title_full_unstemmed |
Characterization of the First Cultured Psychrotolerant Representative of Legionella from Antarctica Reveals Its Unique Genome Structure |
title_sort |
characterization of the first cultured psychrotolerant representative of legionella from antarctica reveals its unique genome structure |
publisher |
American Society for Microbiology |
publishDate |
2021 |
url |
https://doi.org/10.1128/Spectrum.00424-21 https://doaj.org/article/4796c8adcfe74c85863e14d173d55741 |
geographic |
Antarctic |
geographic_facet |
Antarctic |
genre |
Antarc* Antarctic Antarctica |
genre_facet |
Antarc* Antarctic Antarctica |
op_source |
Microbiology Spectrum, Vol 9, Iss 2 (2021) |
op_relation |
https://journals.asm.org/doi/10.1128/Spectrum.00424-21 https://doaj.org/toc/2165-0497 doi:10.1128/Spectrum.00424-21 2165-0497 https://doaj.org/article/4796c8adcfe74c85863e14d173d55741 |
op_doi |
https://doi.org/10.1128/Spectrum.00424-21 |
container_title |
Microbiology Spectrum |
container_volume |
9 |
container_issue |
2 |
_version_ |
1766085717227732992 |