Genomic Insights of Cryobacterium Isolated From Ice Core Reveal Genome Dynamics for Adaptation in Glacier Liu, Yongqin; Shen, Liang; Zeng, Yonghui; Xing, Tingting; Xu, Baiqing; Wang, Ninglian Published in: Frontiers in Microbiology DOI: 10.3389/fmicb.2020.01530 Publication date: 2020 Document version Publisher's PDF, also known as Version of record Document license: CC BY Citation for published version (APA): Liu, Y., Shen, L., Zeng, Y., Xing, T., Xu, B., & Wang, N. (2020). Genomic Insights of Cryobacterium Isolated From Ice Core Reveal Genome Dynamics for Adaptation in Glacier. Frontiers in Microbiology, 11, [1530]. https://doi.org/10.3389/fmicb.2020.01530 Download date: 04. okt.. 2021 fmicb-11-01530 July 11, 2020 Time: 15:35 # 1 ORIGINAL RESEARCH published: 14 July 2020 doi: 10.3389/fmicb.2020.01530 Genomic Insights of Cryobacterium Isolated From Ice Core Reveal Genome Dynamics for Adaptation in Glacier Yongqin Liu1,2,3*, Liang Shen1,4, Yonghui Zeng5, Tingting Xing1,3, Baiqing Xu1,2 and Ninglian Wang2,6 1 Key Laboratory of Tibetan Environment Changes and Land Surface Processes, Institute of Tibetan Plateau Research, Chinese Academy of Sciences, Beijing, China, 2 CAS Center for Excellence in Tibetan Plateau Earth Sciences, Beijing, China, 3 University of Chinese Academy of Sciences, Beijing, China, 4 College of Life Sciences, Anhui Normal University, Wuhu, China, 5 Department of Environmental Science, Aarhus University, Roskilde, Denmark, 6 College of Urban and Environmental Science, Northwest University, Xi’an, China Glacier is the dominant cold habitat in terrestrial environments, providing a model ecosystem to explore extremophilic strategies and study early lives on Earth. The dominant form of life in glaciers is bacteria. However, little is known about past Edited by: evolutionary processes that bacteria underwent during adaptation to the cryosphere David Anthony Pearce, and the connection of their genomic traits to environmental stressors. Aiming to test Northumbria University, the hypothesis that bacterial genomic content and dynamics are driven by glacial United Kingdom environmental stressors, we compared genomes of 21 psychrophilic Cryobacterium Reviewed by: Isao Yumoto, strains, including 14 that we isolated from three Tibetan ice cores, to their National Institute of Advanced mesophilic counterparts from the same family Microbacteriaceae of Actinobacteria. Industrial Science and Technology (AIST), Japan The results show that psychrophilic Cryobacterium underwent more dynamic changes Stefano Raimondi, in genome content, and their genomes have a significantly higher number of University of Modena and Reggio genes involved in stress response, motility, and chemotaxis than their mesophilic Emilia, Italy counterparts (P < 0.05). The phylogenetic birth-and-death model imposed on the *Correspondence: Yongqin Liu phylogenomic tree indicates a vast surge in recent common ancestor of psychrophilic [email protected]; Cryobacterium (gained the greatest number of genes by 1,168) after the division of [email protected] the mesophilic strain Cryobacterium mesophilum. The expansion in genome content Specialty section: brought in key genes primarily of the categories “cofactors, vitamins, prosthetic groups, This article was submitted to pigments,” “monosaccharides metabolism,” and “membrane transport.” The amino acid Extreme Microbiology, a section of the journal substitution rates of psychrophilic Cryobacterium strains are two orders of magnitude Frontiers in Microbiology lower than those in mesophilic strains. However, no significantly higher number of cold Received: 20 December 2019 shock genes was found in psychrophilic Cryobacterium strains, indicating that multi- Accepted: 12 June 2020 copy is not a key factor for cold adaptation in the family Microbacteriaceae, although Published: 14 July 2020 cold shock genes are indispensable for psychrophiles. Extensive gene acquisition and Citation: Liu Y, Shen L, Zeng Y, Xing T, Xu B low amino acid substitution rate might be the strategies of psychrophilic Cryobacterium and Wang N (2020) Genomic Insights to resist low temperature, oligotrophy, and high UV radiation on glaciers. The exploration of Cryobacterium Isolated From Ice Core Reveal Genome Dynamics of genome evolution and survival strategies of psychrophilic Cryobacterium deepens our for Adaptation in Glacier. understanding of bacterial cold adaptation. Front. Microbiol. 11:1530. doi: 10.3389/fmicb.2020.01530 Keywords: glacier, Cryobacterium, genomic, evolutionary processes, cold adaptation Frontiers in Microbiology| www.frontiersin.org 1 July 2020| Volume 11| Article 1530 fmicb-11-01530 July 11, 2020 Time: 15:35 # 2 Liu et al. Genomic Insights of Cryobacterium INTRODUCTION (Liu et al., 2019b). All type strains of Cryobacterium except C. mesophilum described by Dastager et al.(2008) were isolated Glaciers and ice sheets have been recognized as biomes, uniquely from cold environments and recognized as psychrophiles with dominated by microorganisms (Hodson et al., 2008; Anesio and optional growth temperature ranging from 15 to 20◦C and Laybourn-Parry, 2012; Grinsted, 2013). Microbial metabolism growth occurs between 0 and 25◦C. The strain C. mesophilum occurs on glaciers and many community members not only grew between 20 and 28◦C, with optimum growth occurring at perform basal metabolic functions but also grow and divide 25–28◦C(Dastager et al., 2008). Phenotypic analysis showed that (Price, 2000). Microorganisms living in these environments the genus Cryobacterium differed from its Microbacteriaceae have evolved unique features in their proteins, enzyme, counterparts in the presence of a significant amount of 12- membranes, and genetic responses to low temperature and methyl pentadecenoic acid (i.e., a-15:l). The presence of a-15:l is nutrient concentrations and excessive UV radiation (Siddiqui unusual but reasonable for psychrophilic Gram-positive bacteria et al., 2013; De Maayer et al., 2014). in order to maintain membrane fluidity at low temperatures Genomic survival strategies have been investigated in a (Suzuki et al., 1997). few glacial model organisms. Genes encoding proteins with Most of the reported novel Cryobacterium species were known or predicted roles in cold adaptation, i.e., cold-shock isolated from glacial environments (Liu et al., 2018). The protein, proteorhodopsin, osmoprotection, and membrane- culturable bacteria in two ice cores from the Tibetan Plateau were related proteins, were found in genomes of psychrophilic species dominated by Cryobacterium (Liu et al., 2019c). Cryobacterium Flavobacterium bomense sp. nov. isolated from glaciers (Liu et al., exhibited high diversity in more than 10 glaciers around world 2019a). Genome of an ice core strain Dyadobacter tibetensis (Segawa et al., 2005; Liu et al., 2016, 2018), indicating that Y620-1 contained high percentage of new novel genes and Cryobacterium species have developed strategies to endure the genes required for the serine-glyoxylate cycle in one-carbon harsh glacier habitats. Previous studies were most focused metabolism, which may contribute to its survival in glacier on adaptation features of Cryobacterium isolates to cold (Shen et al., 2019). Although glacier bacteria and psychrophiles environments using polyphasic and multilocus sequence analysis from arctic soil are both cold acclimated, glacier bacteria show (Sathyanarayana Reddy et al., 2014; Singh et al., 2015; Lee et al., different genomic adaptation characteristics mainly connected to 2016; Liu et al., 2018). However, a detailed comparative genomic the genes devoted to CRISPR (Clustered Regularly Interspaced study of multiple Cryobacterium genomes is lacking, which Short Palindromic Repeats) defense system, osmotic adaptation, could contribute markedly to and validate our understanding of and metabolism of monosaccharides, nitrogen, and aromatic molecular strategies underlying this genus’ cold adaptation. In compounds, due to the different environmental pressures the present study, we analyzed the genomes of 21 psychrophilic experienced by glacier bacteria and psychrophiles from arctic Cryobacterium isolates of ice core origin in comparison to soils (Shen et al., 2017). The survival strategies of psychrophiles their mesophilic counterparts with the aim to deepen our at the genome level have been well investigated during past understanding of how bacteria adapt to glacial environments. decades (Saunders et al., 2003; Methé et al., 2005; De Maayer Our data suggest that the combination of comparative genomics et al., 2014; Raymond-Bouchard et al., 2018). However, the role of approach and biogeography can be a powerful tool to decipher microevolution, genomic adaptive strategies, and environmental the bacterial cold adaptation mechanisms in psychrophiles. factors in shaping the genomes of bacteria colonizing glaciers are largely unknown. Glaciers not only are the dominant cold habitat to explore the extremophilic strategies in the MATERIALS AND METHODS terrestrial land but also are the representative habitats of early lives on the Earth and perhaps on other planets as well Fourteen psychrophilic Cryobacterium strains were selected (Priscu et al., 2004). from our culture collection including five strains isolated from Species of Cryobacterium are widely distributed in cold the Muztag Ata glacier (named M series, mean annual air environments and well adapted to cold conditions (Liu et al., temperature −4◦C, 36.4◦ N, 87.3◦ E, 6,973 m a.s.l.), three 2018). The genus Cryobacterium, proposed