Genomic diversity and CRISPR-Cas systems in the cyanobacterium Nostoc in the High Arctic.
Journal
Environmental microbiology
ISSN: 1462-2920
Titre abrégé: Environ Microbiol
Pays: England
ID NLM: 100883692
Informations de publication
Date de publication:
06 2021
06 2021
Historique:
received:
14
05
2020
accepted:
22
03
2021
pubmed:
25
3
2021
medline:
16
10
2021
entrez:
24
3
2021
Statut:
ppublish
Résumé
Nostoc (Nostocales, Cyanobacteria) has a global distribution in the Polar Regions. However, the genomic diversity of Nostoc is little known and there are no genomes available for polar Nostoc. Here we carried out the first genomic analysis of the Nostoc commune morphotype with a recent sample from the High Arctic and a herbarium specimen collected during the British Arctic Expedition (1875-76). Comparisons of the polar genomes with 26 present-day non-polar members of the Nostocales family highlighted that there are pronounced genetic variations among Nostoc strains and species. Osmoprotection and other stress genes were found in all Nostoc strains, but the two Arctic strains had markedly higher numbers of biosynthetic gene clusters for uncharacterised non-ribosomal peptide synthetases, suggesting a high diversity of secondary metabolites. Since viral-host interactions contribute to microbial diversity, we analysed the CRISPR-Cas systems in the Arctic and two temperate Nostoc species. There were a large number of unique repeat-spacer arrays in each genome, indicating diverse histories of viral attack. All Nostoc strains had a subtype I-D system, but the polar specimens also showed evidence of a subtype I-B system that has not been previously reported in cyanobacteria, suggesting diverse cyanobacteria-virus interactions in the Arctic.
Identifiants
pubmed: 33760341
doi: 10.1111/1462-2920.15481
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2955-2968Informations de copyright
© 2021 Society for Applied Microbiology and John Wiley & Sons Ltd.
Références
Aguilar, P., Dorador, C., Vila, I., and Sommaruga, R. (2019) Bacterial communities associated with spherical Nostoc macrocolonies. Front Microbiol 10: 483.
Anesio, A.M., Lutz, S., Chrismas, N.A., and Benning, L.G. (2017) The microbiome of glaciers and ice sheets. NPJ Biofilms Microbiomes 3: 1-11.
Barrangou, R., Fremaux, C., Deveau, H., Richards, M., Boyaval, P., Moineau, S., et al. (2007) CRISPR provides acquired resistance against viruses in prokaryotes. Science 315: 1709-1712.
Barria, C., Malecki, M., and Arraiano, C.M. (2013) Bacterial adaptation to cold. Microbiology 159: 2437-2443.
Biller, S.J., Berube, P.M., Lindell, D., and Chisholm, S.W. (2015) Prochlorococcus: the structure and function of collective diversity. Nat Rev Microbiol 13: 13-27.
Biswas, A., Staals, R.H.J., Morales, S.E., Fineran, P., and Brown, C.M. (2016) CRISPRDetect: a flexible algorithm to define CRISPR arrays. BMC Genomics 17: 356.
Blin, K., Shaw, S., Steinke, K., Villebro, R., Ziemert, N., Lee, S.Y., et al. (2019) antiSMASH 5.0: updates to the secondary metabolite genome mining pipeline. Nucleic Acids Res 47: W81-W87.
Boisvert, S., Raymond, F., Godzaridis, E., Laviolette, F., and Corbeil, J. (2012) Ray meta: scalable de novo metagenome assembly and profiling. Genome Biol 13: R122.
Cai, F., Axen, S.D., and Kerfeld, C.A. (2013) Evidence for the widespread distribution of CRISPR-Cas system in the phylum Cyanobacteria. RNA Biol 10: 687-693.
Chénard, C., and Chan, A.M. (2018) Isolation and purification of viruses infecting Cyanobacteria using a liquid bioassat approach. Bio Protocol 8: 1-9.
Chénard, C., Wirth, J.F., and Suttle, C.A. (2016) Viruses infecting a freshwater filamentous Cyanobacterium (Nostoc sp.) encode a functional CRISPR array and a proteobacterial DNA polymerase B. mBio 7: e00667-16.
Chrismas, N.A., Barker, G., Anesio, A.M., and Sánchez-Baracaldo, P. (2016) Genomic mechanisms for cold tolerance and production of exopolysaccharides in the Arctic cyanobacterium Phormidesmis priestleyi. BMC Genomics 17: 533.
Cornet, L., Bertrand, A.R., Hanikenne, M., Javaux, E.J., Wilmotte, A., and Baurain, D. (2018) Metagenomic assembly of new (sub)polar Cyanobacteria and their associated microbiome from non-axenic cultures. Microbial Genomics 4: e000212.
Cubillos-Ruiz, A., Berta-Thompson, J.W., Becker, J.W., van der Donk, W.A., and Chisholm, S.W. (2017) Evolutionary radiation of lanthipeptides in marine cyanobacteria. Proc Natl Acad Sci U S A 114: E5424-E5433.
Dehm, D., Krumbholz, J., Baunach, M., Wiebach, V., Hinrichs, K., Guljamow, A., and Tabuchi, T. (2019) Unlocking the spatial control of secondary metabolism uncovers hidden natural product diversity in Nostoc punctiforme. ACS Chem Biol 14: 1271-1279.
Déraspe, M., Raymond, F., Boisvert, S., Culley, A., Roy, P.H., Laviolette, F., and Corbeil, J. (2017) Phenetic comparison of prokaryotic genomes using k-mers. Mol Biol Evol 1: 2716-2729.
Dickie, G. (1878) On the algae found during the Arctic expedition. J Linn Soc Bot 17: 2-6.
Dion, M., Labrie, S.J., Shah, S.A., and Moineau, S. (2018) CRISPRStudio: a user-friendly software for rapid CRISPR array visualization. Viruses 10: e602.
Elster, J., Lukesová, A., Svoboda, J., Kopecky, J., and Kanda, H. (1999) Diversity and abundance of soil algae in the polar desert, Sverdrup pass, Central Ellesmere Island. Polar Rec 35: 231-254.
Fritsch, F.E. (1917) Freshwater algae. In British Antarctic “Terra Nova” Expedition, London: Natural History Report, British Museum (Natural History), pp. 1-16.
Gatte-Picchi, D., Weiz, A., Ishida, K., Hertweck, C., and Dittmann, E. (2014) Functional analysis of environmental DNA-derived microviridins provides new insights into the diversity of the tricyclic peptide family. Appl Environ Microbiol 80: 1380-1387.
Heidelberg, J.F., Nelson, W.C., Schoenfeld, T., and Bhaya, D. (2009) Germ warfare in a microbial mat community: CRISPRs provide insights into the co-evolution of host and viral genomes. PLoS One 4: e4169.
Hou, S., Brenes-Álvarez, M., Reiman, V., Alkhnbashi, O.S., Backofen, R., Muro-Pastor, A.M., et al. (2019) CRISPR-Cas systems in multicellular cyanobacteria. RNA Biol 16: 518-529.
Huang, I.S., and Zimba, P.V. (2019) Cyanobacterial bioactive metabolites - a review of their chemistry and biology. Harmful Algae 83: 42-94.
Huang, Y., Niu, B., Gao, Y., Fu, L., and Li, W. (2010) CD-HIT suite: a web server for clustering and comparing biological sequences. Bioinformatics 26: 680.
Hyatt, D., Chen, G.L., Locascio, P.F., Land, M.L., Larimer, F.W., and Hauser, L.J. (2010) Prodigal prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11: 119.
Jungblut, A.D., Lovejoy, C., and Vincent, W.F. (2010) Global distribution of cyanobacterial ecotypes in the cold biosphere. ISME J 4: 191-202.
Jungblut, A.D., and Vincent, W.F. (2017) Cyanobacteria in polar and alpine ecosystems. In Psychrophiles: From Biodiversity to Biotechnology, Margesin, R. (ed). Heidelberg: Springer, pp. 181-206.
Leslie, A. (1879) The Arctic Voyages of Adolf Erik Nordenskiöld. London: MacMillan.
Makarova, K.S., Wolf, Y.I., Iranzo, J., Shmakov, S.A., Alkhnabashi, O.S., and Brouns, S.J.J. (2020) Evolutionary classification of CRISPR-Cas systems: a burst of class 2 and derived variants. Nat Rev Microbiol 18: 67-83.
Mazard, S., Penesyan, A., Ostrowski, M., Paulsen, I.T., and Egan, S. (2016) Tiny microbes with a big impact: the role of cyanobacteria and their metabolites in shaping our future. Mar Drugs 14: 97.
Meredith, M., Sommerkorn, M., Cassotta, S., Derksen, C., Ekaykin, A., Hollowed, A., et al. (2019) Polar regions. In IPCC Special Report on the Ocean and Cryosphere in a Changing Climate. Intergovernmental Panel on Climate Change, World Meteorological Organization, Pörtner, H.-O., Roberts, D.C., Masson-Delmotte, V., Zhai, P., Tignor, M., Poloczanska, E., et al. (eds). Geneva: IPCC.
Mohit, V., Culley, A., Lovejoy, C., Bouchard, F., and Vincent, W.F. (2017) Hidden biofilms in a far northern lake and implications for the changing Arctic. NPJ Biofilms Microbiomes 3: 1-3.
Mollenhauer, D., Bengtsson, R., and Lindstrøm, E.-A. (1999) Macroscopic cyanobacteria of the genus Nostoc: a neglected and endangered constituent of European inland aquatic biodiversity. Eur J Phycol 34: 349-360.
Moraes, L.E., Blow, M.B., Hawley, E.R., Piao, H., Chiniquy, J., Shapiro, N., et al. (2017) Resequencing and annotation of the Nostoc punctiforme ATTC 29133 genome: facilitating biofuel and high-value chemical production. AMB EXPRESS 7: 42.
Novis, P.M., and Smissen, R.D. (2006) Two genetic and ecological groups of Nostoc commune in Victoria Land, Antarctica, revealed by AFLP analysis. Antarct Sci 18: 573-581.
Oren, A., and Ventura, S. (2017) The current status of cyanobacterial nomenclature under the “prokaryotic” and the “botanical” code. Antonie Van Leeuwenhoek 110: 1257-1269.
Placzek, S., Schomburg, I., Jeske, L., Ulbrich, M., Tillack, J., and Schomburg, D. (2017) New perspectives and new tools in BRENDA. Nuleic Acids Res 45: D380-D388.
R Core Team. (2013) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing. http://www.R-project.org/.
Raymond, F., Ouameur, A.A., Déaspe, M., Iqbal, N., Gingras, H., Dridi, B., et al. (2016) The initial state of the human gut microbiome determines its reshaping by antibiotics. ISME J 10: 707-720.
Reháková, K., Johansen, J.R., Casamatta, D.A., Xuesong, L., and Vincent, J. (2007) Morphological and molecular characterization of selected desert soil cyanobacteria: three species new to science including Mojavia pulchra gen. et sp. nov. Phycologia 46: 481-502.
Richter, M., and Rosselló-Móra, R. (2009) Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci U S A 106: 19126-19131.
Rodrigues, D.F., and Tiedje, J.M. (2008) Coping with our cold planet. Appl Environ Microbiol 74: 1677-1686.
Sakamoto, T., Yoshida, T., Arima, H., Hatanaka, Y., Takani, Y., and Tamaru, Y. (2009) Accumulation of trehalose in response to desiccation and salt stress in the terrestrial cyanobacterium Nostoc commune. Phycol Res 57: 66-73.
Sánchez-Baracaldo, P. (2015) Origin of marine planktonic cyanobacteria. Sci Rep 5: 17418.
Shannon, P., Markiel, A., Oziers, O., Baliga, N.S., Wang, J.T., Ramage, D., et al. (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13: 2498-2504.
Shih, P.M., Wu, D., Axen, S.D., Fewer, D.P., Talla, E., Calteau, F., et al. (2013) Improving the coverage of the cyanobacterial phylum using diversity-driven genome sequencing. Proc Natl Acad Sci U S A 110: 1053-1058.
Singh, R., Parihar, P., Singh, M., Bajguz, A., Kumar, J., Singh, S., et al. (2017) Uncovering potential applications of cyanobacteria and algal metabolites in biology, agriculture and medicine: current status and future prospects. Front Microbiol 8: 515.
Skinnider, M.A., Merwin, N.J., Johnston, C.W., and Magarvey, N.A. (2017) PRISM 3: expanded prediction of natural product chemical structures from microbial genomes. Nucleic Acids Res 45: W49-W54.
Song, W., Sun, H.-X., Zhang, C., Cheng, L., Peng, Y., Deng, Z., et al. (2019) Prophage hunter: an integrative hunting tool for active prophages. Nucleic Acids Res 47: W74-W80.
Stamatakis, A., Hoover, P., and Rougemont, J. (2008) A rapid bootstrap algorithm for the RAxML web servers. System Biol 57: 758-771.
Suttle, C.A. (2000) Cyanophages and their role in the ecology of cyanobacteria. In The Ecology of Cyanobacteria: Their Diversity in Time and Space, Whitton, M.A., and Potts, M. (eds). Boston: Kluwer Academic Publishers, pp. 563-589.
Tamaru, Y., Takani, Y., Yoshida, T., and Sakamoto, T. (2005) Crucial role of extracellular polysaccharides in desiccation and freezing tolerance in the terrestrial cyanobacterium Nostoc commune. Appl Environ Microbiol 7: 7327-7333.
Varin, T., Lovejoy, C., Jungblut, A.D., Vincent, W.F., and Corbeil, J. (2012) Metagenomic analysis of stress genes in microbial mat communities from Antarctica and the high Arctic. Appl Environ Microbiol 78: 549-559.
Welker, M., and von Döhren, H. (2006) Cyanobacterial peptides - nature's own combinatorial biosynthesis. FEMS Microbiol Ecol 30: 530-563.
Wright, D., Pricett, T., Helm, R.F., and Potts, M. (2001) Form species Nostoc commune (Cyanobacteria). Int J Syst Evol Microbiol 51: 1839-1852.
Wright, D.J., Smith, S.C., Joardar, V., Scherer, S., Jervis, J., Warren, A., et al. (2005) UV irradiation and desiccation modulate the three-dimensional extracellular matrix of Nostoc commune (Cyanobacteria). J Biol Chem 280: 40271-40281.