Characterization of the First Cultured Psychrotolerant Representative of Legionella from Antarctica Reveals Its Unique Genome Structure

• 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: Legionella; psychrotolerant; insertion sequence; horizontal gene transfer; comparative genomic analysis; cellular fatty acids; Microbiology; QR1-502; Antarctic; Antarc*; Antarctica
• Online Access: https://doi.org/10.1128/Spectrum.00424-21; https://doaj.org/article/4796c8adcfe74c85863e14d173d55741

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 ...