Search
Close this search box.

Effect of salinity on scytonemin yield in endolithic cyanobacteria from the Atacama Desert – Scientific Reports

  • Neifar, M., Maktouf, S., Ghorbel, R. E., Jaouani, A. & Cherif, A. Extremophiles as source of novel bioactive compounds with industrial potential. In Biotechnology of Bioactive Compounds: Sources and Applications (eds Gupta, V. K. et al.) 245–267 (Wiley Blackwell, 2015).

    Chapter 

    Google Scholar
     

  • Núñez-Montero, K. & Barrientos, L. Advances in antarctic research for antimicrobial discovery: A comprehensive narrative review of bacteria from antarctic environments as potential sources of novel antibiotic compounds against human pathogens and microorganisms of industrial importance. Antibiotics 7, 90. https://doi.org/10.3390/antibiotics7040090 (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Okoro, C. K. et al. Diversity of culturable actinomycetes in hyper-arid soils of the Atacama Desert, Chile. Antonie van Leeuwenhoek Int. J. Gen. Mol. Microbiol. 95, 121–133 (2009).

    Article 

    Google Scholar
     

  • Bratchkova, A. & Ivanova, V. Bioactive metabolites produced by microorganisms collected in Antarctica and the Arctic. Biotechnol. Biotechnol. Equip. 25, 1–7. https://doi.org/10.5504/bbeq.2011.0116 (2011).

    Article 

    Google Scholar
     

  • Diffey, B. L. Solar ultraviolet radiation effects on biological systems. Phys. Med. Biol. 36, 299 (1991).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Rastogi, R. P. & Incharoensakdi, A. Characterization of UV-screening compounds, mycosporine-like amino acids, and scytonemin in the cyanobacterium Lyngbya sp. CU2555. FEMS Microbiol. Ecol. 87, 244–256 (2014).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Rastogi, R. P., Madamwar, D. & Incharoensakdi, A. Sun-screening bioactive compounds mycosporine-like amino acids in naturally occurring cyanobacterial biofilms: Role in photoprotection. J. Appl. Microbiol. 119, 753–762 (2015).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Proteau, P. J., Gerwick, W. H., Garcia-Pichel, F. & Castenholz, R. The structure of scytonemin, an ultraviolet sunscreen pigment from the sheaths of cyanobacteria. Experientia 49, 825 (1993).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Garcia-Pichel, F. & Castenholz, R. W. Characterization and biological implications of scytonemin, a cyanobacterial sheath pigment. J. Phycol. 27, 395–409 (1991).

    Article 
    CAS 

    Google Scholar
     

  • Dillon, J. G., Tatsumi, C. M., Tandingan, P. G. & Castenholz, R. W. Effect of environmental factors on the synthesis of scytonemin, a UV-screening pigment, in a cyanobacterium (Chroococcidiopsis sp.). Arch. Microbiol. 177, 322–331 (2002).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Fleming, E. D. & Castenholz, R. W. Effects of periodic desiccation on the synthesis of the UV-screening compound, scytonemin, in cyanobacteria. Environ. Microbiol. 9, 1448–1455 (2007).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Rath, J., Mandal, S. & Adhikary, S. P. Salinity induced synthesis of UV-screening compound scytonemin in the cyanobacterium Lyngbya aestuarii. J. Photochem. Photobiol. B 115, 5–8 (2012).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Singh, H. Desiccation and radiation stress tolerance in cyanobacteria. J. Basic Microbiol. 58, 813–826. https://doi.org/10.1002/jobm.201800216 (2018).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Soule, T., Stout, V., Swingley, W. D., Meeks, J. C. & Garcia-Pichel, F. Molecular genetics and genomic analysis of scytonemin biosynthesis in Nostoc punctiforme ATCC 29133. J. Bacteriol. 189, 4465–4472 (2007).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Klicki, K. et al. The widely conserved ebo cluster is involved in precursor transport to the periplasm during scytonemin synthesis in Nostoc punctiforme. Mbio 9(10), 2018. https://doi.org/10.1128/mBio (2018).

    Article 

    Google Scholar
     

  • D’Agostino, P. M. et al. Bioinformatic, phylogenetic and chemical analysis of the UV-absorbing compounds scytonemin and mycosporine-like amino acids from the microbial mat communities of Shark Bay, Australia. Environ. Microbiol. 21, 702–715 (2019).

    Article 
    PubMed 

    Google Scholar
     

  • Balskus, E. P. & Walsh, C. T. An enzymatic cyclopentyl[b]indole formation involved in scytonemin biosynthesis. J. Am. Chem. Soc. 131, 14648–14649 (2009).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Pathak, J. et al. Cyanobacterial secondary metabolite scytonemin: A potential photoprotective and pharmaceutical compound. Proc. Natl Acad. Sci. India Sect. B Biol. Sci. 90, 467–481. https://doi.org/10.1007/s40011-019-01134-5 (2020).

    Article 
    CAS 

    Google Scholar
     

  • Duan, Z. et al. Lentiviral shRNA screen of human kinases identifies PLK1 as a potential therapeutic target for osteosarcoma. Cancer Lett. 293, 220–229 (2010).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Zhang, G., Zhang, Z. & Liu, Z. Scytonemin inhibits cell proliferation and arrests cell cycle through downregulating Plk1 activity in multiple myeloma cells. Tumor Biol. 34, 2241–2247 (2013).

    Article 
    CAS 

    Google Scholar
     

  • Wierzchos, J. et al. Adaptation strategies of endolithic chlorophototrophs to survive the hyperarid and extreme solar radiation environment of the Atacama Desert. Front. Microbiol. 6, 934 (2015).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Vítek, P. et al. Distribution of scytonemin in endolithic microbial communities from halite crusts in the hyperarid zone of the Atacama Desert, Chile. FEMS Microbiol. Ecol. 90, 351–366 (2014).

    PubMed 

    Google Scholar
     

  • Cordero, R. R. et al. Ultraviolet radiation in the Atacama Desert. Antonie van Leeuwenhoek Int. J. Gen. Mol. Microbiol. 111, 1301–1313 (2018).

    Article 
    CAS 

    Google Scholar
     

  • Wierzchos, J., Casero, M. C., Artieda, O. & Ascaso, C. Endolithic microbial habitats as refuges for life in polyextreme environment of the Atacama Desert. Curr. Opin. Microbiol. 43, 124–131. https://doi.org/10.1016/j.mib.2018.01.003 (2018).

    Article 
    PubMed 

    Google Scholar
     

  • Casero, M. C., Ascaso, C., Quesada, A., Mazur-Marzec, H. & Wierzchos, J. Response of endolithic chroococcidiopsis strains from the polyextreme Atacama Desert to light radiation. Front. Microbiol. 11, 614875 (2021).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Casero, M. C. et al. The composition of endolithic communities in gypcrete is determined by the specific microhabitat architecture. Biogeosciences 18, 993–1007 (2021).

    Article 
    ADS 
    CAS 

    Google Scholar
     

  • Davila, A. F. et al. In situ metabolism in halite endolithic microbial communities of the hyperarid Atacama Desert. Front. Microbiol. 6, 153663 (2015).

    Article 

    Google Scholar
     

  • Olsson-Francis, K. & Cockell, C. S. Use of cyanobacteria for in-situ resource use in space applications. Planet Space Sci. 58, 1279–1285 (2010).

    Article 
    ADS 
    CAS 

    Google Scholar
     

  • Melero-Jiménez, I. J., Martín-Clemente, E., García-Sánchez, M. J., Bañares-España, E. & Flores-Moya, A. The limit of resistance to salinity in the freshwater cyanobacterium Microcystis aeruginosa is modulated by the rate of salinity increase. Ecol. Evol. 10, 5045–5055 (2020).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Thomas, M. K. & Litchman, E. Effects of temperature and nitrogen availability on the growth of invasive and native cyanobacteria. Hydrobiologia 763, 357–369 (2016).

    Article 

    Google Scholar
     

  • von Alvensleben, N., Stookey, K., Magnusson, M. & Heimann, K. Salinity tolerance of Picochlorum atomus and the use of salinity for contamination control by the freshwater cyanobacterium Pseudanabaena limnetica. PLoS ONE 8, e63569 (2013).

    Article 
    ADS 

    Google Scholar
     

  • Moisander, P. H., McClinton, E. & Paerl, H. W. Salinity effects on growth, photosynthetic parameters, and nitrogenase activity in estuarine planktonic cyanobacteria. Microb. Ecol. 43, 432–442 (2002).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • Singh, J., Tripathi, R. & Thakur, I. S. Characterization of endolithic cyanobacterial strain, Leptolyngbya sp. ISTCY101, for prospective recycling of CO2 and biodiesel production. Bioresour. Technol. 166, 345–352 (2014).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Ozturk, S. & Aslim, B. Modification of exopolysaccharide composition and production by three cyanobacterial isolates under salt stress. Environ. Sci. Pollut. Res. 17, 595–602 (2010).

    Article 
    CAS 

    Google Scholar
     

  • Bemal, S. & Anil, A. C. Effects of salinity on cellular growth and exopolysaccharide production of freshwater Synechococcus strain CCAP1405. J. Plank. Res. 40, 46–58 (2018).

    Article 
    CAS 

    Google Scholar
     

  • Gao, X. Scytonemin plays a potential role in stabilizing the exopolysaccharidic matrix in terrestrial cyanobacteria. Microb. Ecol. 73, 255–258 (2017).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • Singh, S. P., Kumari, S., Rastogi, R. P., Singh, K. L. & Sinha, R. P. Photoprotective and biotechnological potentials of cyanobacterial sheath pigment, scytonemin. Afr. J. Biotechnol. 9, 580–588 (2010).

    CAS 

    Google Scholar
     

  • Velu, C., Cirés, S., Alvarez-Roa, C. & Heimann, K. First outdoor cultivation of the N2-fixing cyanobacterium Tolypothrix sp. in low-cost suspension and biofilm systems in tropical Australia. J. Appl. Phycol. 27, 1743–1753 (2015).

    Article 
    CAS 

    Google Scholar
     

  • Mirón, A. S., Gómez, A. C., Camacho, F. G., Grima, E. M. & Chisti, Y. Comparative evaluation of compact photobioreactors for large-scale monoculture of microalgae. In Progress in Industrial Microbiology Vol. 35 (eds Osinga, R. et al.) 249–270 (Elsevier, 1999).


    Google Scholar
     

  • Chini Zittelli, G., Rodolfi, L., Biondi, N. & Tredici, M. R. Productivity and photosynthetic efficiency of outdoor cultures of Tetraselmis suecica in annular columns. Aquaculture 261, 932–943 (2006).

    Article 

    Google Scholar
     

  • Borowitzka, M. A. & Moheimani, N. R. Open pond culture systems. In Algae for Biofuels and Energy (eds Borowitzka, M. A. & Moheimani, N. R.) 133–152 (Springer, 2013).

    Chapter 

    Google Scholar
     

  • Moreno, J., Vargas, M. Á., Rodríguez, H., Rivas, J. & Guerrero, M. G. Outdoor cultivation of a nitrogen-fixing marine cyanobacterium, Anabaena sp. ATCC 33047. Biomol. Eng. 20, 191–197 (2003).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Chini Zittelli, G., Lauceri, R., Faraloni, C., Silva Benavides, A. M. & Torzillo, G. Valuable pigments from microalgae: Phycobiliproteins, primary carotenoids, and fucoxanthin. Photochem. Photobiol. Sci. https://doi.org/10.1007/s43630-023-00407-3 (2023).

    Article 
    PubMed 

    Google Scholar
     

  • Chen, Z. et al. Genomic and transcriptomic insights into the habitat adaptation of the diazotrophic paddy-field cyanobacterium Nostoc sphaeroides. Environ. Microbiol. 23, 5802–5822 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Tippelt, A., Busche, T., Rückert, C. & Nett, M. Complete genome sequence of the cryptophycin-producing cyanobacterium Nostoc sp. strain ATCC 53789. Microbiol. Resour. Announc. 9, 10 (2020).

    Article 

    Google Scholar
     

  • Fidor, A. et al. Nostoc edaphicum CCNP1411 from the Baltic Sea—A new producer of nostocyclopeptides. Mar. Drugs 18, 442 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Soule, T. et al. A comparative genomics approach to understanding the biosynthesis of the sunscreen scytonemin in cyanobacteria. BMC Genom. 10, 1–10 (2009).

    Article 

    Google Scholar
     

  • Teikari, J. E., Hou, S., Wahlsten, M., Hess, W. R. & Sivonen, K. Comparative genomics of the Baltic Sea toxic cyanobacteria Nodularia spumigena UHCC 0039 and its response to varying salinity. Front. Microbiol. 9, 299361 (2018).

    Article 

    Google Scholar
     

  • Voß, B. et al. Insights into the physiology and ecology of the brackish-water-adapted cyanobacterium Nodularia spumigena CCY9414 based on a genome-transcriptome analysis. PLoS ONE 8, e60224 (2013).

    Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Rippka, E., Deruelles, J. & Waterbury, N. B. Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J. Gen. Microbiol. 111, 1 (1979).


    Google Scholar
     

  • Garcia-Pichel, F., Sherry, N. D. & Castenholz, R. W. Evidence for an ultraviolet sunscreen role of the extracellular pigment scytonemin in the terrestrial cyanobacterium Chiorogloeopsis sp.. Photochem. Photobiol. 56, 17–23 (1992).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Cirés, S., Wörmer, L., Timón, J., Wiedner, C. & Quesada, A. Cylindrospermopsin production and release by the potentially invasive cyanobacterium Aphanizomenon ovalisporum under temperature and light gradients. Harmful Algae 10, 668–675 (2011).

    Article 

    Google Scholar
     

  • Singh, S., Verma, E., Niveshika, T. B. & Mishra, A. K. Exopolysaccharide production in Anabaena sp. PCC 7120 under different CaCl2 regimes. Physiol. Mol. Biol. Plants 22(4), 557–566 (2016).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Dubois, M., Gilles, K. A., Hamilton, J. K., Roberts, P. A. & Smith, F. Colorimetric method for the determination of sugars and related substances. Anal. Chem. 28, 350–356 (1956).

    Article 
    CAS 

    Google Scholar
     

  • Thompson, J. D., Higgins, D. G. & Gibson, T. J. CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673–4680 (1994).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Tamura, K., Stecher, G. & Kumar, S. MEGA11: Molecular evolutionary genetics analysis version 11. Mol. Biol. Evol. 38, 3022–3027 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Tamura, K. Estimation of the Number of Nucleotide Substitutions When There are Strong Transition-Transversion and G+C-Content Biases. https://academic.oup.com/mbe/article/9/4/678/1254082 (1992).