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Environmental Adaptation of Psychrophilic Bacteria Subtercola spp. Isolated from Various Cryospheric Habitats

  • Microbial Ecology and Environmental Microbiology
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Abstract

Subtercola boreus K300T is a novel psychrophilic strain that was isolated from permanently cold groundwater in Finland and has also been found in several places in Antarctica including lake, soil, and rocks. We performed genomic and transcriptomic analyses of 5 strains from Antarctica and a type strain to understand their adaptation to different environments. Interestingly, the isolates from rocks showed a low growth rate and smaller genome size than strains from the other isolation sources (lake, soil, and groundwater). Based on these habitat-dependent characteristics, the strains could be classified into two ecotypes, which showed differences in energy production, signal transduction, and transcription in the clusters of orthologous groups of proteins (COGs) functional category. In addition, expression pattern changes revealed differences in metabolic processes, including uric acid metabolism, DNA repair, major facilitator superfamily (MFS) transporters, and xylose degradation, depending on the nutritional status of their habitats. These findings provide crucial insights into the environmental adaptation of bacteria, highlighting genetic diversity and regulatory mechanisms that enable them to thrive in the cryosphere.

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Data availability

The sequences of 6 strains reported in this paper have been deposited in the GenBank database (BioProject no. PRJNA378458).

References

  • Aguilar, P. S., Cronan, J. E., Jr., & de Mendoza, D. (1998). A Bacillus subtilis gene induced by cold shock encodes a membrane phospholipid desaturase. Journal of Bacteriology, 180, 2194–2200.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baker-Austin, C., & Dopson, M. (2007). Life in acid: PH homeostasis in acidophiles. Trends in Microbiology, 15, 165–171.

    Article  CAS  PubMed  Google Scholar 

  • Bankevich, A., Nurk, S., Antipov, D., Gurevich, A. A., Dvorkin, M., Kulikov, A. S., Lesin, V. M., Nikolenko, S. I., Pham, S., Prjibelski, A. D., et al. (2012). SPAdes: A new genome assembly algorithm and its applications to single-cell sequencing. Journal of Computational Biology, 19, 455–477.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baraúna, R. A., Freitas, D. Y., Pinheiro, J. C., Folador, A. R., & Silva, A. (2017). A proteomic perspective on the bacterial adaptation to cold: Integrating OMICs data of the psychrotrophic bacterium Exiguobacterium antarcticum B7. Proteomes, 5, 9.

    Article  PubMed  PubMed Central  Google Scholar 

  • Barria, C., Malecki, M., & Arraiano, C. M. (2013). Bacterial adaptation to cold. Microbiology, 159, 2437–2443.

    Article  CAS  PubMed  Google Scholar 

  • Bolger, A. M., Lohse, M., & Usadel, B. (2014). Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics, 30, 2114–2120.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burger, A. E., Lindeboom, H. J., & Williams, A. J. (1971). The mineral and energy contributions of guano of selected species of birds to the Marion Island terrestrial ecosystem. South African Journal of Antarctic Research, 8, 59–70.

    Google Scholar 

  • Cary, S. C., McDonald, I. R., Barrett, J. E., & Cowan, D. A. (2010). On the rocks: The microbiology of Antarctic Dry Valley soils. Nature Reviews Microbiology, 8, 129–138.

    Article  CAS  PubMed  Google Scholar 

  • Cordero, O. X., & Hogeweg, P. (2009). The impact of long-distance horizontal gene transfer on prokaryotic genome size. Proceedings of the National Academy of Sciences, 106, 21748–21753.

    Article  CAS  Google Scholar 

  • Deming, J. W. (2002). Psychrophiles and polar regions. Current Opinion in Microbiology, 5, 301–309.

    Article  CAS  PubMed  Google Scholar 

  • Ding, W., Baumdicker, F., & Neher, R. A. (2018). panX: Pan-genome analysis and exploration. Nucleic Acids Research, 46, e5.

    Article  PubMed  Google Scholar 

  • Emms, D. M., & Kelly, S. (2015). OrthoFinder: Solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biology, 16, 157.

    Article  PubMed  PubMed Central  Google Scholar 

  • Garrity, G. (2007). Bergey’s manual® of Systematic bacteriology: volume 2: the proteobacteria, part B: the Gammaproteobacteria. New York: Springer.

    Google Scholar 

  • Gianese, G., Argos, P., & Pascarella, S. (2001). Structural adaptation of enzymes to low temperatures. Protein Engneering, 14, 141–148.

    Article  CAS  Google Scholar 

  • Hammann, R., & Kutzner, H. J. (1998). Key enzymes for the degradation of benzoate, m- and p-hydroxybenzoate by some members of the order Actinomycetales. Journal of Basic Microbiology, 38, 207–220.

    Article  CAS  PubMed  Google Scholar 

  • Hessen, D. O., Jeyasingh, P. D., Neiman, M., & Weider, L. J. (2010). Genome streamlining and the elemental costs of growth. Trends in Ecology & Evolution, 25, 75–80.

    Article  Google Scholar 

  • Horikoshi, K. (1999). Alkaliphiles: Some applications of their products for biotechnology. Microbiology and Molecular Biology Reviews, 63, 735–750.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hunt, M., Silva, N. D., Otto, T. D., Parkhill, J., Keane, J. A., & Harris, S. R. (2015). Circlator: Automated circularization of genome assemblies using long sequencing reads. Genome Biology, 16, 294.

    Article  PubMed  PubMed Central  Google Scholar 

  • Jaenicke, R., & Bohm, G. (1998). The stability of proteins in extreme environments. Current Opinion in Structural Biology, 8, 738–748.

    Article  CAS  PubMed  Google Scholar 

  • Keto-Timonen, R., Hietala, N., Palonen, E., Hakakorpi, A., Lindstrom, M., & Korkeala, H. (2016). Cold shock proteins: A minireview with special emphasis on Csp-family of enteropathogenic Yersinia. Frontiers in Microbiology, 7, 1151.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kim, H., Lee, J. Y., & Lee, K. K. (2014). Thermal characteristics and bacterial diversity of forest soil in the Haean basin of Korea. Scientific World Journal, 2014, 247401.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kim, J. H., Ahn, I. Y., Lee, K. S., Chung, H. S., & Choi, H. G. (2007). Vegetation of Barton Peninsula in the neighbourhood of King Sejong Station (King George Island, maritime Antarctic). Polar Biology, 30, 903–916.

    Article  Google Scholar 

  • Kim, O. S., Chae, N., Lim, H. S., Cho, A., Kim, J. H., Hong, S. G., & Oh, J. (2012a). Bacterial diversity in ornithogenic soils compared to mineral soils on King George Island, Antarctica. Journal of Microbiology, 50, 1081–1085.

    Article  CAS  PubMed  Google Scholar 

  • Kim, O. S., Cho, Y. J., Lee, K., Yoon, S. H., Kim, M., Na, H., Park, S. C., Jeon, Y. S., Lee, J. H., Yi, H., et al. (2012b). Introducing EzTaxon-e: A prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. International Journal of Systematic and Evolutionary Microbiology, 62, 716–721.

    Article  CAS  PubMed  Google Scholar 

  • Kumar, A., Alam, A., Tripathi, D., Rani, M., Khatoon, H., Pandey, S., Ehtesham, N. Z., & Hasnain, S. E. (2018). Protein adaptations in extremophiles: An insight into extremophilic connection of mycobacterial proteome. Seminars in Cell & Developmental Biology, 84, 147–157.

    Article  CAS  Google Scholar 

  • Kumar, S., Stecher, G., & Tamura, K. (2016). MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33, 1870–1874.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kurokawa, M., Seno, S., Matsuda, H., & Ying, B. W. (2016). Correlation between genome reduction and bacterial growth. DNA Research, 23, 517–525.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Langmead, B., & Salzberg, S. L. (2012). Fast gapped-read alignment with Bowtie 2. Nature Methods, 9, 357–359.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee, J., Cho, J., Cho, Y. J., Cho, A., Woo, J., Lee, J., Hong, S. G., Sul, W. J., & Kim, O. S. (2019). The latitudinal gradient in rock-inhabiting bacterial community compositions in Victoria Land, Antarctica. Science of the Total Environment, 657, 731–738.

    Article  CAS  PubMed  Google Scholar 

  • Lee, Y. M., Kim, G., Jung, Y. J., Choe, C. D., Yim, J. H., Lee, H. K., & Hong, S. G. (2012). Polar and alpine microbial collection (PAMC): A culture collection dedicated to polar and alpine microorganisms. Polar Biology, 35, 1433–1438.

    Article  Google Scholar 

  • Liao, Y., Smyth, G. K., & Shi, W. (2013). The Subread aligner: Fast, accurate and scalable read mapping by seed-and-vote. Nucleic Acids Research, 41, e108.

    Article  PubMed  PubMed Central  Google Scholar 

  • Love, M. I., Huber, W., & Anders, S. (2014). Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology, 15, 550.

    Article  PubMed  PubMed Central  Google Scholar 

  • Männistö, M., Schumann, P., Rainey, F., Kämpfer, P., Tsitko, I., Tiirola, M., & Salkinoja-Salonen, M. (2000). Subtercola boreus gen. nov., sp. nov. and Subtercola frigoramans sp. nov., two new psychrophilic actinobacteria isolated from boreal groundwater. International Journal of Systematic and Evolutionary Microbiology, 50, 1731–1739.

    Article  PubMed  Google Scholar 

  • Margesin, R., & Miteva, V. (2011). Diversity and ecology of psychrophilic microorganisms. Research in Microbiology, 162, 346–361.

    Article  PubMed  Google Scholar 

  • Markkula, A., Lindström, M., Johansson, P., Björkroth, J., & Korkeala, H. (2012). Roles of four putative DEAD-box RNA helicase genes in growth of Listeria monocytogenes EGD-e under heat, pH, osmotic, ethanol, and oxidative stress conditions. Applied and Environmental Microbiology, 78, 6875–6882.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mocali, S., Chiellini, C., Fabiani, A., Decuzzi, S., de Pascale, D., Parrilli, E., Tutino, M. L., Perrin, E., Bosi, E., Fondi, M., et al. (2017). Ecology of cold environments: New insights of bacterial metabolic adaptation through an integrated genomic-phenomic approach. Scientific Reports, 7, 839.

    Article  PubMed  PubMed Central  Google Scholar 

  • Qin, Q. L., Xie, B. B., Yu, Y., Shu, Y. L., Rong, J. C., Zhang, Y. J., Zhao, D. L., Chen, X. L., Zhang, X. Y., Chen, B., et al. (2014). Comparative genomics of the marine bacterial genus Glaciecola reveals the high degree of genomic diversity and genomic characteristic for cold adaptation. Environmental Microbiology, 16, 1642–1653.

    Article  CAS  PubMed  Google Scholar 

  • Ribaudo, R., Gilman, M., Kingston, R. E., Choczynski, P., & Sacchi, N. (2001). Preparation of RNA from tissues and cells. Current Protocols in Immunology. https://doi.org/10.1002/0471142735.im1011s04

    Article  PubMed  Google Scholar 

  • Richter, M., Rosselló-Móra, R., Oliver Glöckner, F., & Peplies, J. (2016). JSpeciesWS: A web server for prokaryotic species circumscription based on pairwise genome comparison. Bioinformatics, 32, 929–931.

    Article  CAS  PubMed  Google Scholar 

  • Si, H. L., Shi, F. X., Zhang, L. L., Yue, H. S., Wang, H. Y., & Zhao, Z. T. (2017). Subtercola lobariae sp. nov., an actinobacterium of the family Microbacteriaceae isolated from the lichen Lobaria retigera. International Journal of Systematic and Evolutionary Microbiology, 67, 1516–1521.

    Article  CAS  PubMed  Google Scholar 

  • Steven, B., Léveillé, R., Pollard, W. H., & Whyte, L. G. (2006). Microbial ecology and biodiversity in permafrost. Extremophiles, 10, 259–267.

    Article  PubMed  Google Scholar 

  • Tamura, K., & Nei, M. (1993). Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution, 10, 512–526.

    CAS  PubMed  Google Scholar 

  • Tatusova, T., DiCuccio, M., Badretdin, A., Chetvernin, V., Nawrocki, E. P., Zaslavsky, L., Lomsadze, A., Pruitt, K. D., Borodovsky, M., & Ostell, J. (2016). NCBI prokaryotic genome annotation pipeline. Nucleic Acids Research, 44, 6614–6624.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Treseder, K. K., & Lennonb, J. T. (2015). Fungal traits that drive ecosystem dynamics on land. Microbiology and Molecular Biology Reviews, 79, 243–262.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • van de Vossenberg, J. L., Driessen, A. J., & Konings, W. N. (1998a). The essence of being extremophilic: The role of the unique archaeal membrane lipids. Extremophiles, 2, 163–170.

    Article  PubMed  Google Scholar 

  • van de Vossenberg, J. L., Driessen, A. J., Zillig, W., & Konings, W. N. (1998b). Bioenergetics and cytoplasmic membrane stability of the extremely acidophilic, thermophilic archaeon Picrophilus oshimae. Extremophiles, 2, 67–74.

    Article  PubMed  Google Scholar 

  • Wiegel, J., & Kevbrin, V. V. (2004). Alkalithermophiles. Biochemical Society Transactions, 32, 193–198.

    Article  CAS  PubMed  Google Scholar 

  • Wiegeshoff, F., Beckering, C. L., Debarbouille, M., & Marahiel, M. A. (2006). Sigma L is important for cold shock adaptation of Bacillus subtilis. Journal of Bacteriology, 188, 3130–3133.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was supported by a Grant from the Korea Polar Research Institute (PE23130).

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Correspondence to Ok-Sun Kim.

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Lee, H., Cho, YJ., Cho, A. et al. Environmental Adaptation of Psychrophilic Bacteria Subtercola spp. Isolated from Various Cryospheric Habitats. J Microbiol. 61, 663–672 (2023). https://doi.org/10.1007/s12275-023-00068-y

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