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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Published in:Microbiology Spectrum
Main Authors: Sho Shimada, Ryosuke Nakai, Kotaro Aoki, Sakae Kudoh, Satoshi Imura, Norifumi Shimoeda, Giichiro Ohno, Kentaro Watanabe, Yasunari Miyazaki, Yoshikazu Ishii, Kazuhiro Tateda
Format: Article in Journal/Newspaper
Language:English
Published: American Society for Microbiology 2021
Subjects:
Online Access:https://doi.org/10.1128/Spectrum.00424-21
https://doaj.org/article/4796c8adcfe74c85863e14d173d55741
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spelling 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
institution Open Polar
collection 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
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