Skip to main content
Log in

Possible involvement of extracellular polymeric substrates of Antarctic cyanobacterium Nostoc sp. strain SO-36 in adaptation to harsh environments

  • Regular Paper – Physiology/Biochemistry/Molecular and Cellular Biology
  • Published:
Journal of Plant Research Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Cabanettes F, Klopp C (2018) D-GENIES: dot plot large genomes in an interactive, efficient and simple way. PeerJ 6:e4958

    Article  PubMed  PubMed Central  Google Scholar 

  • Cavacini P (2001) Soil algae from northern Victoria Land (Antarctica). Polar Biosci 14:45–60

    Google Scholar 

  • 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Chrismas NAM, Anesio AM, Sanchez-Baracaldo P (2018) The future of genomics in polar and alpine cyanobacteria. FEMS Microbiol Ecol 94:fiy032

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Dyer DL, Gafford RD (1961) Some characteristics of a thermophilic blue-green alga. Science 134:616–617

    Article  PubMed  CAS  Google Scholar 

  • Elhai J, Wolk CP (1988) Conjugal transfer of DNA to cyanobacteria. Methods Enzymol 167:747–754

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Gagunashvili AN, Andresson OS (2018) Distinctive characters of Nostoc genomes in cyanolichens. BMC Genomics 19:434

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gurevich A, Saveliev V, Vyahhi N, Tesler G (2013) QUAST: quality assessment tool for genome assemblies. Bioinformatics 29:1072–1075

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Kolmogorov M, Yuan J, Lin Y, Pevzner PA (2019) Assembly of long, error-prone reads using repeat graphs. Nat Biotechnol 37:540–546

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Los DA, Murata N (1999) Responses to cold shock in cyanobacteria. J Mol Microbiol Biotechnol 1:221–230

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • Roberson EB, Firestone MK (1992) Relationship between Desiccation and Exopolysaccharide Production in a Soil Pseudomonas sp. Appl Environ Microbiol 58:1284–1291

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rossi F, De Philippis R (2015) Role of cyanobacterial exopolysaccharides in phototrophic biofilms and in complex microbial mats. Life (basel) 5:1218–1238

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Schmid J, Sieber V, Rehm B (2015) Bacterial exopolysaccharides: biosynthesis pathways and engineering strategies. Front Microbiol 6:496

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  CAS  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. Mol Biol Evol 10:512–526

    PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Tanizawa Y, Fujisawa T, Nakamura Y (2018) DFAST: a flexible prokaryotic genome annotation pipeline for faster genome publication. Bioinformatics 34:1037–1039

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Wick RR, Schultz MB, Zobel J, Holt KE (2015) Bandage: interactive visualization of de novo genome assemblies. Bioinformatics 31:3350–3352

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yamada S, Ohkubo S, Miyashita H, Setoguchi H (2012) Genetic diversity of symbiotic cyanobacteria in Cycas revoluta (Cycadaceae). FEMS Microbiol Ecol 81:696–706

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

Download references

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

Authors

Corresponding author

Correspondence to Yu Kanesaki.

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.

Supplementary file1 (PDF 327 KB)

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.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10265-022-01411-x

Keywords

Navigation