Abstract
Cyanobacteria are some of the primary producers in extremely cold biospheres such as the Arctic, Antarctic, and vast ice sheets. Many genera of cyanobacteria are identified from these harsh environments, but their specific mechanisms for cold adaptation are not fully understood. Nostoc sp. strain SO-36 is a cyanobacterium isolated in Antarctica more than 30 years ago and regarded as a psychrotolelant species. To determine whether the strain is psychrotolelant or psychrophilic, it was first grown at 30 °C and 10 °C. The cells grew exponentially at 30 °C, but their growth stopped at 10 °C, indicating that the strain is only psychrotolerant. Microscopic analysis revealed that the morphology of the cells grown at 30 °C was filamentous and differentiated heterocysts, which are specialized cells for gaseous nitrogen fixation under nitrogen-deprived conditions, indicating that the strain can grow diazotrophically. The cells grown at 10 °C have a smaller size, shortened filament length and decreased chlorophyll content per cell. At 10 °C, the cells are aggregated with extracellular polymeric substrates (EPSs), which is a common mechanism to protect cells from ultraviolet light. These results imply that segmentation into short filaments was induced by photodamage at low temperatures. To fully understand the adaptation mechanisms of Nostoc sp. strain SO-36 for low-temperature conditions, next-generation sequencing analyses were conducted. Complete genome sequence of the strain revealed that it has one main chromosome of approximately 6.8 Mbp with 4 plasmids, including 6855 coding sequences, 48 tRNA genes, 4 copies of rRNA operons, and 5 CRISPR regions. Putative genes for EPS biosynthesis were found to be conserved in Nostocaceae regardless of their habitat. These results provide basic information to understand the adaptation mechanisms at low temperatures, and the strain can be a model organism to analyze adaptation to extreme environments.
Similar content being viewed by others
References
Arima H, Horiguchi N, Takaichi S, Kofuji R, Ishida K, Wada K, Sakamoto T (2012) Molecular genetic and chemotaxonomic characterization of the terrestrial cyanobacterium Nostoc commune and its neighboring species. FEMS Microbiol Ecol 79:34–45
Arnon DI, McSwain BD, Tsujimoto HY, Wada K (1974) Photochemical activity and components of membrane preparations from blue-green algae. I. Coexistence of two photosystems in relation to chlorophyll a and removal of phycocyanin. Biochim Biophys Acta 357:231–245
Awai K, Watanabe H, Benning C, Nishida I (2007) Digalactosyldiacylglycerol is required for better photosynthetic growth of Synechocystis sp. PCC6803 under phosphate limitation. Plant Cell Physiol 48:1517–1523
Bagchi SN, Dubey N, Singh P (2017) Phylogenetically distant clade of Nostoc-like taxa with the description of Aliinostoc gen. nov. and Aliinostoc morphoplasticum sp. nov. Int J Syst Evol Microbiol 67:3329–3338
Bell-Doyon P, Laroche J, Saltonstall K, Villarreal Aguilar JC (2020) Specialized bacteriome uncovered in the coralloid roots of the epiphytic gymnosperm, Zamia pseudoparasitica. Environmental DNA 2:418–428
Bhagat N, Raghav M, Dubey S, Namita Bedi N (2021) Bacterial exopolysaccharides: Insight into their role in plant abiotic stress tolerance. J Microbiol Biotechnol 31:1045–1059
Biondi N, Tredici MR, Taton A, Wilmotte A, Hodgson DA, Losi D, Marinelli F (2008) Cyanobacteria from benthic mats of Antarctic lakes as a source of new bioactivities. J Appl Microbiol 105:105–115
Cabanettes F, Klopp C (2018) D-GENIES: dot plot large genomes in an interactive, efficient and simple way. PeerJ 6:e4958
Cavacini P (2001) Soil algae from northern Victoria Land (Antarctica). Polar Biosci 14:45–60
Chintalapati S, Prakash JS, Gupta P, Ohtani S, Suzuki I, Sakamoto T, Murata N, Shivaji S (2006) A novel Delta9 acyl-lipid desaturase, DesC2, from cyanobacteria acts on fatty acids esterified to the sn-2 position of glycerolipids. Biochem J 398:207–214
Chintalapati S, Prakash JSS, Singh AK, Ohtani S, Suzuki I, Murata N, Shivaji S (2007) Desaturase genes in a psychrotolerant Nostoc sp. are constitutively expressed at low temperature. Biochem Biophys Res Commun 362:81–87
Chrismas NAM, Anesio AM, Sanchez-Baracaldo P (2018) The future of genomics in polar and alpine cyanobacteria. FEMS Microbiol Ecol 94:fiy032
Di Pippo F, Ellwood NTW, Gismondi A, Bruno L, Rossi F, Magni P, De Philippis R (2013) Characterization of exopolysaccharides produced by seven biofilm-forming cyanobacterial strains for biotechnological applications. J Appl Phycol 25:1697–1708
DuBois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356
Dyer DL, Gafford RD (1961) Some characteristics of a thermophilic blue-green alga. Science 134:616–617
Elhai J, Wolk CP (1988) Conjugal transfer of DNA to cyanobacteria. Methods Enzymol 167:747–754
Fujisawa T, Narikawa R, Maeda SI, Watanabe S, Kanesaki Y, Kobayashi K, Nomata J, Hanaoka M, Watanabe M, Ehira S, Suzuki E, Awai K, Nakamura Y (2017) CyanoBase: a large-scale update on its 20th anniversary. Nucleic Acids Res 45:D551–D554
Gagunashvili AN, Andresson OS (2018) Distinctive characters of Nostoc genomes in cyanolichens. BMC Genomics 19:434
Gombos Z, Wada H, Murata N (1994) The recovery of photosynthesis from low-temperature photoinhibition is accelerated by the unsaturation of membrane lipids: a mechanism of chilling tolerance. Proc Natl Acad Sci U S A 91:8787–8791
Gurevich A, Saveliev V, Vyahhi N, Tesler G (2013) QUAST: quality assessment tool for genome assemblies. Bioinformatics 29:1072–1075
Hashidoko Y, Nishizuka H, Tanaka M, Murata K, Murai Y, Hashimoto M (2019) Isolation and characterization of 1-palmitoyl-2-linoleoyl-sn-glycerol as a hormogonium-inducing factor (HIF) from the coralloid roots of Cycas revoluta (Cycadaceae). Sci Rep 9:4751
Kanesaki Y, Hirose M, Hirose Y, Fujisawa T, Nakamura Y, Watanabe S, Matsunaga S, Uchida H, Murakami A (2018) Draft genome sequence of the nitrogen-fixing and hormogonia-inducing cyanobacterium Nostoc cycadae strain WK-1, isolated from the coralloid roots of Cycas revoluta. Genome Announc 6:e00021-e118
Kolmogorov M, Yuan J, Lin Y, Pevzner PA (2019) Assembly of long, error-prone reads using repeat graphs. Nat Biotechnol 37:540–546
Krembs C, Eickenb H, Jungea K, Deming JW (2002) High concentrations of exopolymeric substances in Arctic winter sea ice: implications for the polar ocean carbon cycle and cryoprotection of diatom. Deep-Sea Res I 49:2163–2181
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549
Los DA, Murata N (1999) Responses to cold shock in cyanobacteria. J Mol Microbiol Biotechnol 1:221–230
Maeda K, Okuda Y, Enomoto G, Watanabe S, Ikeuchi M (2021) Biosynthesis of a sulfated exopolysaccharide, synechan, and bloom formation in the model cyanobacterium Synechocystis sp. strain PCC 6803. Elife 10:e66538
Morgan-Kiss RM, Priscu JC, Pocock T, Gudynaite-Savitch L, Huner NP (2006) Adaptation and acclimation of photosynthetic microorganisms to permanently cold environments. Microbiol Mol Biol Rev 70:222–252
Nishii K, Möller M, Hart M (2019) DNA extraction protocol for long read sequencing; DNA extraction for state-of-the-art sequencing. Botanic Stories of Royal Botanic Garden Edinburgh, vol. 2022 https://stories.rbge.org.uk/archives/30792. Accessed 5 May 2022
Ohtani S (1986) Epiphytic algae on mosses in the vicinity of Syowa Station, Antarctica. Men Natl Inst Polar Res 44:209–219
Ohtani S, Akiyama M, Kanda H (1991) Analysis of Antarctic soil algae by the direct observation using the contact slide method. Antarct Rec 35:285–295
Papaefthimiou D, Hrouzek P, Mugnai MA, Lukesova A, Turicchia S, Rasmussen U, Ventura S (2008) Differential patterns of evolution and distribution of the symbiotic behaviour in nostocacean cyanobacteria. Int J Syst Evol Microbiol 58:553–564
Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW (2015) CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res 25:1043–1055
Pereira SB, Mota R, Santos CL, De Philippis R, Tamagnini P (2013) Assembly and export of extracellular polymeric substances (EPS) in cyanobacteria: a phylogenomic approach. Adv Bot Res 65:235–279
Rajaniemi P, Hrouzek P, Kastovska K, Willame R, Rantala A, Hoffmann L, Komarek J, Sivonen K (2005) Phylogenetic and morphological evaluation of the genera Anabaena, Aphanizomenon, Trichormus and Nostoc (Nostocales, Cyanobacteria). Int J Syst Evol Microbiol 55:11–26
Ran L, Larsson J, Vigil-Stenman T, Nylander JA, Ininbergs K, Zheng WW, Lapidus A, Lowry S, Haselkorn R, Bergman B (2010) Genome erosion in a nitrogen-fixing vertically transmitted endosymbiotic multicellular cyanobacterium. PLoS ONE 5:e11486
Řeháková K, Johansen JR, Casamatta DA, Xuesong L, 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
Roberson EB, Firestone MK (1992) Relationship between Desiccation and Exopolysaccharide Production in a Soil Pseudomonas sp. Appl Environ Microbiol 58:1284–1291
Rossi F, De Philippis R (2015) Role of cyanobacterial exopolysaccharides in phototrophic biofilms and in complex microbial mats. Life (basel) 5:1218–1238
Sakamoto T, Hashimoto A, Yamaba M, Wada N, Yoshida T, Inoue-Sakamoto K, Nishiuchi T, Matsugo S (2019) Four chemotypes of the terrestrial cyanobacterium Nostoc commune characterized by differences in the mycosporine-like amino acids. Phycol Res 67:3–11
Schmid J, Sieber V, Rehm B (2015) Bacterial exopolysaccharides: biosynthesis pathways and engineering strategies. Front Microbiol 6:496
Singh SM, Elster J (2007) Cyanobacteria in Antarctic Lake Environments. In: Seckbach J (ed) Algae and cyanobacteria in extreme environments. Springer Netherlands, Dordrecht, pp 303–320
Souza HA, Muller LA, Brandao RL, Lovato MB (2012) Isolation of high quality and polysaccharide-free DNA from leaves of Dimorphandra mollis (Leguminosae), a tree from the Brazilian Cerrado. Genet Mol Res 11:756–764
Stanier RY, Kunisawa R, Mandel M, Cohen-Bazire G (1971) Purification and properties of unicellular blue-green algae (order Chroococcales). Bacteriol Rev 35:171–205
Suzuki I, Kanesaki Y, Mikami K, Kanehisa M, Murata N (2001) Cold-regulated genes under control of the cold sensor Hik33 in Synechocystis. Mol Microbiol 40:235–244
Tamaru Y, Takani Y, Yoshida T, Sakamoto T (2005) Crucial role of extracellular polysaccharides in desiccation and freezing tolerance in the terrestrial cyanobacterium Nostoc commune. Appl Environ Microbiol 71:7327–7333
Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526
Tang EPY, Tremblay R, Vincent WF (1997) Cyanobacterial dominance of polar freshwater ecosystems: Are high-latitude mat-formers adapted to low temperature? J Phycol 33:171–181
Tanizawa Y, Fujisawa T, Nakamura Y (2018) DFAST: a flexible prokaryotic genome annotation pipeline for faster genome publication. Bioinformatics 34:1037–1039
Wada H, Gombos Z, Murata N (1990) Enhancement of chilling tolerance of a cyanobacterium by genetic manipulation of fatty acid desaturation. Nature 347:200–203
Wellburn AR (1994) The spectral determination of Chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J Plant Physiol 144:307–313
Wick RR, Schultz MB, Zobel J, Holt KE (2015) Bandage: interactive visualization of de novo genome assemblies. Bioinformatics 31:3350–3352
Yamada S, Ohkubo S, Miyashita H, Setoguchi H (2012) Genetic diversity of symbiotic cyanobacteria in Cycas revoluta (Cycadaceae). FEMS Microbiol Ecol 81:696–706
Zippel B, Neu TR (2011) Characterization of glycoconjugates of extracellular polymeric substances in tufa-associated biofilms by using fluorescence lectin-binding analysis. Appl Environ Microbiol 77:505–516
Acknowledgements
This work was partly supported by MEXT/JSPS KAKENHI Grant Number 18H03941 and 20K06683 for KA, 20K05724 for TS; 21K05338 for YK; Research Institute of Green Science and Technology Fund for Research Project Support (2021RIGST-21B02) for YK and Joint Research Program for Faculties of Science and Agriculture for KA from National University Corporation Shizuoka University.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Effendi, D.B., Sakamoto, T., Ohtani, S. et al. Possible involvement of extracellular polymeric substrates of Antarctic cyanobacterium Nostoc sp. strain SO-36 in adaptation to harsh environments. J Plant Res 135, 771–784 (2022). https://doi.org/10.1007/s10265-022-01411-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10265-022-01411-x