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Fischerella thermalis: a model organism to study thermophilic diazotrophy, photosynthesis and multicellularity in cyanobacteria

  • Jaime Alcorta
  • Pablo Vergara-Barros
  • Laura A. Antonaru
  • María E. Alcamán-Arias
  • Dennis J. Nürnberg
  • Beatriz DíezEmail author
Review

Abstract

The true-branching cyanobacterium Fischerella thermalis (also known as Mastigocladus laminosus) is widely distributed in hot springs around the world. Morphologically, it has been described as early as 1837. However, its taxonomic placement remains controversial. F. thermalis belongs to the same genus as mesophilic Fischerella species but forms a monophyletic clade of thermophilic Fischerella strains and sequences from hot springs. Their recent divergence from freshwater or soil true-branching species and the ongoing process of specialization inside the thermal gradient make them an interesting evolutionary model to study. F. thermalis is one of the most complex prokaryotes. It forms a cellular network in which the main trichome and branches exchange metabolites and regulators via septal junctions. This species can adapt to a variety of environmental conditions, with its photosynthetic apparatus remaining active in a temperature range from 15 to 58 °C. Together with its nitrogen-fixing ability, this allows it to dominate in hot spring microbial mats and contribute significantly to the de novo carbon and nitrogen input. Here, we review the current knowledge on the taxonomy and distribution of F. thermalis, its morphological complexity, and its physiological adaptations to an extreme environment.

Keywords

Fischerella Mastigocladus Distribution Thermophile Nitrogen fixation Photosynthesis Multicellularity Hot springs 

Notes

Acknowledgements

This work was financially supported by FONDECYT regular N° 1150171 and 1190998. MEA-A was supported by Postdoctoral fellowship FONDECYT N° 3170807. JA was supported by the Doctoral fellowship from CONICYT N° 21191763; PVB by a VRI-PUC Scholarship; LAA by an Imperial College Schrödinger Scholarship; DJN by the BBSRC (Grant BB/R001383/1).

Compliance with ethical standards

Conflict of interest

Authors declare they do not have conflict of interest.

Supplementary material

792_2019_1125_MOESM1_ESM.docx (2.9 mb)
Supplementary material 1 (DOCX 2949 kb)

References

  1. Alcamán ME, Fernández C, Delgado A, Bergman B, Díez B (2015) The cyanobacterium Mastigocladus fulfills the nitrogen demand of a terrestrial hot spring microbial mat. ISME J 9(10):2290–2303.  https://doi.org/10.1038/ismej.2015.63 CrossRefGoogle Scholar
  2. Alcamán ME, Alcorta J, Bergman B, Vásquez M, Polz M, Díez B (2017) Physiological and gene expression responses to nitrogen regimes and temperatures in Mastigocladus sp. strain CHP1, a predominant thermotolerant cyanobacterium of hot springs. Syst Appl Microbiol 40(2):102–113.  https://doi.org/10.1016/j.syapm.2016.11.007 CrossRefPubMedGoogle Scholar
  3. Alcamán-Arias ME, Pedrós-Alió C, Tamames J, Fernández C, Pérez-Pantoja D, Vásquez M, Díez B (2018) Diurnal changes in active carbon and nitrogen pathways along the temperature gradient in Porcelana hot spring microbial mat. Front Microbiol 9:2353.  https://doi.org/10.3389/fmicb.2018.02353 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Alcorta J, Espinoza S, Viver T, Alcamán-Arias ME, Trefault N, Rosselló-Móra R, Díez B (2018) Temperature modulates Fischerella thermalis ecotypes in Porcelana hot spring. Syst Appl Microbiol 41(6):531–543.  https://doi.org/10.1016/j.syapm.2018.05.006 CrossRefPubMedGoogle Scholar
  5. Allen JF (2004) Cytochrome b6f: structure for signalling and vectorial metabolism. Trends Plant Sci 9(3):130–137.  https://doi.org/10.1016/j.tplants.2004.01.009 CrossRefPubMedGoogle Scholar
  6. Almog O, Shoham G, Michaeli D, Nechushtai R (1991) Monomeric and trimeric forms of photosystem I reaction center of Mastigocladus laminosus: crystallization and preliminary characterization. Proc Natl Acad Sci USA 88(12):5312–5316.  https://doi.org/10.1073/pnas.88.12.5312 CrossRefPubMedGoogle Scholar
  7. Anagnostidis K, Komárek J (1990) Modern approach to the classification system of Cyanophytes 5– Stigonematales. Arch Hydrobiol 86(suppl):1–73Google Scholar
  8. Antonaru LA, Nürnberg DJ (2017) Role of PatS and cell type on the heterocyst spacing pattern in a filamentous branching cyanobacterium. FEMS Microbiol Lett.  https://doi.org/10.1093/femsle/fnx154 CrossRefPubMedPubMedCentralGoogle Scholar
  9. Awai K, Lechno-Yossef S, Wolk CP (2009) Heterocyst envelope glycolipids. In lipids in photosynthesis. Springer, Dordrecht, pp 179–202CrossRefGoogle Scholar
  10. Baniulis D, Yamashita E, Zhang H, Hasan SS, Cramer WA (2008) Structure-function of the cytochrome b6f complex. J Photochem Photobiol 84(6):1349–1358.  https://doi.org/10.1111/j.1751-1097.2008.00444.x CrossRefGoogle Scholar
  11. Billaud VA (1967) Aspects of the nitrogen nutrition of some naturally occurring populations of blue-green algae. In: Environmental requirements of blue–green Algae. Federal Water Pollution Control Administration, Corvalis, USA, pp 35–53Google Scholar
  12. Bohler M, Binder A (1980) Photosynthetic Activities of a membrane preparation of the thermophilic cyanobacterium Mastigocladus laminosus. Arch Microbiol 124:155–160.  https://doi.org/10.1007/BF00427721 CrossRefGoogle Scholar
  13. Bolhuis H, Cretoiu MS, Stal LJ (2014) Molecular ecology of microbial mats. FEMS Microbiol Ecol 90(2):335–350.  https://doi.org/10.1111/1574-6941.12408 CrossRefPubMedGoogle Scholar
  14. Boomer S, Noll K, Geesey G, Dutton BE (2009) Formation of multilayered photosynthetic biofilms en an alkaline thermal spring in Yellowstone National Park, Wyoming. Appl Environ Microbiol 75:2464–2475.  https://doi.org/10.1128/AEM.01802-08 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Bornet E, Flahault CH (1886) Revision des Nosocacees heterocystees contenues dans les principaux herbiers de France. Ann des Sci Nat Bot 3:323–381Google Scholar
  16. Bornet E, Flahault CH (1887) Revision des Nosocacees heterocystees contenues dans les principaux herbiers de France. Ann des Sci Nat Bot 5:51–129Google Scholar
  17. Brock TD (1967) Relationship between standing crop and primary productivity along a hot spring thermal gradient. Ecology 48(4):566–571.  https://doi.org/10.2307/1936500 CrossRefGoogle Scholar
  18. Brock TD, Brock ML (1966) Temperature optima for algal development in Yellowstone and Iceland hot springs. Nature 209(5024):733.  https://doi.org/10.1038/209733a0 CrossRefGoogle Scholar
  19. Chalanika De Silva HC, Asaeda T (2017) Effects of heat stress on growth, photosynthetic pigments, oxidative damage and competitive capacity of three submerged macrophytes. J Plant Interact 12(1):228–236.  https://doi.org/10.1080/17429145.2017.1322153 CrossRefGoogle Scholar
  20. Cohn F (1862) Ueber die Algen des Karlsbader Sprudels, mit Rucksicht auf die Bildung des Sprudelsinters. Abhandlungen der Schesischen Gesellschaft fur vaterlandische Kultur 2:35–55Google Scholar
  21. Dagan T, Roettger M, Stucken K, Landan G, Koch R, Major P, Gould SB, Goremykin VV, Rippka R, Tandeau de Marsac N, Gugger M, Lockhart PJ, Allen JF, Brune I, Maus I, Puhler A, Martin WF (2013) Genomes of Stigonematalean cyanobacteria (subsection V) and the evolution of oxygenic photosynthesis from prokaryotes to plastids. Genome Biol Evol 5:31–44.  https://doi.org/10.1093/gbe/evs117 CrossRefPubMedGoogle Scholar
  22. Drouet F (1981) Revision of the Stigonemataceae with a summary of the classification of the blue–green algae. Nova Hedwigia 66:1–221Google Scholar
  23. Duerring M, Huber R, Bode W, Ruembeli R, Zuber H (1990) Refined three-dimensional structure of phycoerythrocyanin from the cyanobacterium Mastigocladus laminosus at 2.7 Å. J Mol Biol 211(3):633–644.  https://doi.org/10.1016/0022-2836(90)90270-v CrossRefPubMedGoogle Scholar
  24. Finsinger K, Scholz I, Serrano A, Morales S, Uribe-Lorio L, Mora M, Sittenfield A, Weckesser J, Hess W (2008) Characterization of true-branching cyanobacteria from geothermal sites and hot springs of Costa Rica. Environ Microbiol 10:460–473.  https://doi.org/10.1111/j.1462-2920.2007.01467.x CrossRefPubMedGoogle Scholar
  25. Fish A, Danieli T, Ohad I, Nechushtai R, Livnah O (2005) Structural basis for the thermostability of ferredoxin from the cyanobacterium Mastigocladus laminosus. J Mol Biol 350(3):599–608.  https://doi.org/10.1016/j.jmb.2005.04.071 CrossRefPubMedGoogle Scholar
  26. Flores E, Herrero A (2010) Compartmentalized function through cell differentiation in filamentous cyanobacteria. Nat Rev Microbiol 8:39–50.  https://doi.org/10.1038/nrmicro2242 CrossRefPubMedGoogle Scholar
  27. Flores E, Pernil R, Muro-Pastor AM, Mariscal V, Maldener I, Lechno-Yossef S, Fan Q, Wolk P, Herrero A (2007) Septum-localized protein required for filament integrity and diazotrophy in the heterocyst-forming cyanobacterium Anabaena sp. strain PCC 7120. J Bacteriol 189(10):3884–3890.  https://doi.org/10.1128/JB.00085-07 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Flores E, Nieves-Morión M, Mullineaux C (2019) Cyanobacterial septal junctions: properties and regulation. Life 9(1):1.  https://doi.org/10.3390/life9010001 CrossRefGoogle Scholar
  29. Fogg GE (1951) Studies on nitrogen fixation by blue–green algae: II. Nitrogen fixation by Mastigocladus laminosus Cohn. J Exp Bot 2(1):117–120.  https://doi.org/10.1093/jxb/2.1.117 CrossRefGoogle Scholar
  30. Frémy P (1930) Lex Myxophyceés de l’ Afrique équatoriale francaise. Archives de Botanique, Tom. III., Mém 2:1–507Google Scholar
  31. Frémy MP (1936) Remarques sur la morphologie et la biologie de l’Hapalosiphon laminosus Hansg. Ann Protistol 5:175–200Google Scholar
  32. Fricke HC, Wing SL (2004) Oxygen isotope and paleobotanical estimates of temperature and δ18O–latitude gradients over North America during the early Eocene. Am J Sci 304(7):612–635.  https://doi.org/10.2475/ajs.304.7.612 CrossRefGoogle Scholar
  33. Gan F, Bryant DA (2015) Adaptive and acclimative responses of cyanobacteria to far-red light. Environ Microbiol 17(10):3450–3465.  https://doi.org/10.1111/1462-2920.12992 CrossRefPubMedGoogle Scholar
  34. Gan F, Zhang S, Rockwell NC, Martin SS, Lagarias JC, Bryant DA (2014) Extensive remodeling of a cyanobacterial photosynthetic apparatus in far-red light. Science 345(6202):1312–1317.  https://doi.org/10.1126/science.1256963 CrossRefPubMedGoogle Scholar
  35. Geitler L (1932) Cyanophyceae. In: Abenhorst L (ed) Kryptogamenflora von Deutschland, Österreich und der Schweiz, vol 14. Koeltz Scientific Books, Königstein, p 1196Google Scholar
  36. Glauser M, Bryant DA, Frank G, Wehrli E, Rusconi SS, Sidler W, Zuber H (1992) Phycobilisome structure in the cyanobacteria Mastigocladus laminosus and Anabaena sp. PCC 7120. Eur J Biochem 205(3):907–915.  https://doi.org/10.1111/j.1432-1033.1992.tb16857.x CrossRefPubMedGoogle Scholar
  37. Golubic S, Hernandez-Marine M, Hoffmann L (1996) Developmental aspects of branching in filamentous Cyanophyta/Cyanobacteria. Arch Hydrobiol Algol Stud 117:303–329Google Scholar
  38. Gomont M (1895) Note sur le Scytonema ambiguum Kütz. J de Bot 9:49–53Google Scholar
  39. Gonzalez-Esquer CR, Smarda J, Rippka R, Axen SD, Guglielmi G, Gugger M, Kerfeld CA (2016) Cyanobacterial ultrastructure in light of genomic sequence data. Photosynth Res 129(2):147–157.  https://doi.org/10.1007/s11120-016-0286-2 CrossRefPubMedGoogle Scholar
  40. Gugger MF, Hoffmann L (2004) Polyphyly of true branching cyanobacteria (Stigonematales). Int J Syst Evol Microbiol 54(2):349–357.  https://doi.org/10.1099/ijs.0.02744-0 CrossRefPubMedGoogle Scholar
  41. Hansgirg A (1885) Über den polymorphismus der algen. Bot Centralblatt 22:385–406Google Scholar
  42. Herrero A, Stavans J, Flores E (2016) The multicellular nature of filamentous heterocyst-forming cyanobacteria. FEMS Microbiol Rev 40(6):831–854.  https://doi.org/10.1093/femsre/fuw029 CrossRefPubMedGoogle Scholar
  43. Ho MY, Shen G, Canniffe DP, Zhao C, Bryant DA (2016) Light-dependent chlorophyll f synthase is a highly divergent paralog of PsbA of photosystem II. Science.  https://doi.org/10.1126/science.aaf9178 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Hutchins PR, Miller SR (2017) Genomics of variation in nitrogen fixation activity in a population of the thermophilic cyanobacterium Mastigocladus laminosus. ISME J 11(1):78.  https://doi.org/10.1038/ismej.2016.105 CrossRefPubMedGoogle Scholar
  45. Kastovský J, Johansen J (2008) Mastigocladus laminosus (Stigonematales, Cyanobacteria): phylogenetic relationship of strains from thermal springs to soil-inhabiting genera of the order and taxonomic implications for the genus. Phycologia 43:307–320CrossRefGoogle Scholar
  46. Kim Y, Joachimiak G, Ye Z, Binkowski TA, Zhang R, Gornicki P, Callahan SM, Hess WR, Haselkorn R, Joachimiak A (2011) Structure of transcription factor HetR required for heterocyst differentiation in cyanobacteria. Proc Natl Acad Sci USA 108(25):10109–10114.  https://doi.org/10.1073/pnas.1106840108 CrossRefPubMedGoogle Scholar
  47. Kirchner O (1898) Schizophyceae. In: Engler A, Prantl K (Eds) Die natürlichen Pflantzenfamilien, I. Teil, Abteilung Ia pp. 45–92. Leipzig, GermanyGoogle Scholar
  48. Koch R, Kupczok A, Stucken K, Ilhan J, Hammerschmidt K, Dagan T (2017) Plasticity first: molecular signatures of a complex morphological trait in filamentous cyanobacteria. BMC Evol Biol 17(1):209.  https://doi.org/10.1186/s12862-017-1053-5 CrossRefPubMedPubMedCentralGoogle Scholar
  49. Komárek j (2013) Süßwasserflora von Mitteleuropa, Bd. 19/3: Cyanoprokaryota. 3. Teil/3rd part: Heterocytous Genera. Süßwasserflora von Mitteleuropa. Spektrum Academischer Verlag, HeidelbergCrossRefGoogle Scholar
  50. Komárek J, Kaštovský J, Mareš J, Johansen JR (2014) Taxonomic classification of cyanoprokaryotes (cyanobacterial genera) 2014, using a polyphasic approach. Preslia 86:295–335Google Scholar
  51. Kurisu G, Zhang H, Smith JL, Cramer WA (2003) Structure of the cytochrome b6f complex of oxygenic photosynthesis: tuning the cavity. Science 302:1009–1014.  https://doi.org/10.1126/science.1090165 CrossRefPubMedGoogle Scholar
  52. Lacap D, Barraquio W, Pointing S (2007) Thermophilic microbial mats in a tropical geothermal location display pronounced seasonal changes but appear resilient to stochastic disturbance. Environ Microbiol 9:3065–3076.  https://doi.org/10.1111/j.1462-2920.2007.01417.x CrossRefPubMedGoogle Scholar
  53. Larkum AWD, Szabó M, Fitzpatrick D, Raven JA (2017) Cyclic electron flow in cyanobacteria and eukaryotic algae. In: Barber J, Ruban AV (eds) Photosynthesis and bioenergetics. World Scientific Publishing, Singapore, pp 305–343CrossRefGoogle Scholar
  54. Lehner J, Berendt S, Dörsam B, Pérez R, Forchhammer K, Maldener I (2013) Prokaryotic multicellularity: a nanopore array for bacterial cell communication. FASEB J 27(6):2293–2300.  https://doi.org/10.1096/fj.12-225854 CrossRefPubMedGoogle Scholar
  55. Li M, Calteau A, Semchonok DA, Witt TA, Nguyen JT, Sassoon N, Sassoon N, Boekema EJ, Whitelegge J, Gugger M, Bruce B (2019) Physiological and evolutionary implications of tetrameric photosystem I In cyanobacteria. bioRxiv.  https://doi.org/10.1101/544353 CrossRefGoogle Scholar
  56. Löwenstein A (1903) Über die Temperaturgrenzen des Lebens bei der Thermalalge Mastigocladus laminosus Cohn. Ber dtsch Bot Ges 21:317–323Google Scholar
  57. Lushy A, He Z, Fish A, Darash-Yahana M, Minai L, Verchovsky L, Michaeli D, Nechushtai R (2000) An insight into the assembly and organization of Photosystem I complex in thylakoid membranes of the thermophilic cyanobacterium, Mastigocladus laminosus. Indian J Biochem Biophys 37(6):405–417PubMedGoogle Scholar
  58. Mackenzie R, Pedrós-Alió C, Díez B (2013) Bacterial composition of microbial mats in hot springs in Northern Patagonia: variations with seasons and temperature. Extremophiles 17:123–136.  https://doi.org/10.1007/s00792-012-0499-z CrossRefPubMedGoogle Scholar
  59. Marcenko E (1962) Licht- und elektronenmikroskopische Untersuchungen an der Thermalalge Mastigocladus laminosus Cohn. Acta Bot Coratica 20(21):47–74Google Scholar
  60. Mariscal V (2014) Cell-cell joining proteins in heterocyst-forming cyanobacteria. In: Flores E, Herrero A (eds) The cell biology of cyanobacteria. Caister Academic Press, Poole, UK, pp 293–304Google Scholar
  61. Melick DR, Broady PA, Rowan KS (1991) Morphological and physiological characteristics of a non-heterocystous strain of the cyanobacterium Mastigocladus laminosus Cohn from fumarolic soil on Mt Erebus, Antarctica. Polar Biol 11(2):81–89.  https://doi.org/10.1007/BF00234270 CrossRefGoogle Scholar
  62. Miller S, Purugganan M, Curtis S (2006) Molecular population genetics and phenotypic diversification of two populations of the thermophilic cyanobacterium Mastigocladus laminosus. Appl Environ Microbiol 72:2793–2800.  https://doi.org/10.1128/AEM.72.4.2793-2800.2006 CrossRefPubMedPubMedCentralGoogle Scholar
  63. Miller S, Castenholz R, Pedersen D (2007) Phylogeography of the thermophilic cyanobacterium Mastigocladus laminosus. Appl Environ Microbiol 73:4751–4759.  https://doi.org/10.1128/AEM.02945-06 CrossRefPubMedPubMedCentralGoogle Scholar
  64. Miller SR, Williams C, Strong AL, Carvey D (2009) Ecological specialization in a spatially structured population of the thermophilic cyanobacterium Mastigocladus laminosus. Appl Environ Microbiol 75(3):729–734.  https://doi.org/10.1128/AEM.01901-08 CrossRefPubMedGoogle Scholar
  65. Mullineaux CW, Mariscal V, Nenninger A, Khanum H, Herrero A, Flores E, Adams DG (2008) Mechanism of intercellular molecular exchange in heterocyst forming cyanobacteria. EMBO J 27:1299–1308.  https://doi.org/10.1038/emboj.2008.66 CrossRefPubMedPubMedCentralGoogle Scholar
  66. Muster P, Binder A, Schneider K, Bachofen R (1983) Influence of temperature and pH on the growth of the thermophilic cyanobacterium Mastigocladus laminosus in continuous culture. Plant Cell Physiol 24(2):273–280.  https://doi.org/10.1093/pcp/24.2.273 CrossRefGoogle Scholar
  67. Nayar AS, Yamaura H, Rajagopalan R, Risser DD, Callahan SM (2007) FraG is necessary for filament integrity and heterocyst maturation in the cyanobacterium Anabaena sp. strain PCC 7120. Microbiology 153:601–607.  https://doi.org/10.1099/mic.0.2006/002535-0 CrossRefPubMedGoogle Scholar
  68. Nierzwicki SA, Maratea D, Balkwill DL, Hardie LP, Mehta VB, Stevens SE (1982) Ultrastructure of the cyanobacterium, Mastigocladus laminosus. Arch Microbiol 133(1):11–19.  https://doi.org/10.1007/BF00943762 CrossRefGoogle Scholar
  69. Nierzwicki-Bauer SA, Balkwill DL, Stevens SE (1984) Heterocyst differentiation in the cyanobacterium Mastigocladus laminosus. J Bacteriol 157(2):514–525PubMedPubMedCentralGoogle Scholar
  70. Nies M, Wehrmeyer W (1981) Biliprotein assembly in the hemidiseoidal phycobilisomes of the thermophilic cyanobacterium Mastigocladus laminosus Cohn. Characterization of dissociation products with special reference to the peripheral phycoerythrocyanin–phycocyanin complexes. Arch Microbiol 129:374–379.  https://doi.org/10.1007/BF00406466 CrossRefGoogle Scholar
  71. Nürnberg DJ, Mariscal V, Parker J, Mastroianni G, Flores E, Mullineaux CW (2014) Branching and intercellular communication in the section V cyanobacterium Mastigocladus laminosus, a complex multicellular prokaryote. Mol Microbiol 91(5):935–949.  https://doi.org/10.1111/mmi.12506 CrossRefPubMedGoogle Scholar
  72. Parks DH, Chuvochina M, Waite DW, Rinke C, Skarshewski A, Chaumel P, Hugenholtz P (2018) A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Nat Biotechnol 36:996–1004.  https://doi.org/10.1038/nbt.4229 CrossRefPubMedGoogle Scholar
  73. Radway J, Weissman J, Wilde E, Benemann J (1992) Exposure of Fischerella [Mastigocladus] to high and low temperature extremes: strain evaluation for a thermal mitigation process. J Appl Phycol 4(1):67–77.  https://doi.org/10.1007/BF00003962 CrossRefGoogle Scholar
  74. Ramesh VM, Fish A, Michaeli D, Keren N, Ohad I, Vorchovsky L, Nechushtai R (2002) Isolation and characterization of an oxygen evolving photosystem 2 core complex from the thermophilic cyanobacterium Mastigocladus laminosus. Photosynthetica 40(3):355–361.  https://doi.org/10.1023/A:1022666706700 CrossRefGoogle Scholar
  75. Reuter W, Nickel-Reuter C (1992) Molecular assembly of the phycobilisomes from the cyanobacterium Mastigocladus laminosus. J Photochem Photobiol B 18(1):51–66.  https://doi.org/10.1016/1011-1344(93)80040-G CrossRefGoogle Scholar
  76. Reuter W, Wiegand G, Huber R, Than ME (1999) Structural analysis at 2.2 Å of orthorhombic crystals presents the asymmetry of the allophycocyanin–linker complex, AP LC7. 8, from phycobilisomes of Mastigocladus laminosus. Proc Natl Acad Sci USA 96(4):1363–1368CrossRefPubMedGoogle Scholar
  77. Richter M, Rosselló-Móra R (2009) Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci USA 106(45):19126–19131.  https://doi.org/10.1073/pnas.0906412106 CrossRefPubMedGoogle Scholar
  78. Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RY (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. Microbiology 111(1):1–61.  https://doi.org/10.1099/00221287-111-1-1 CrossRefGoogle Scholar
  79. Roeselers G, Norris T, Castenholz R, Rysgaard S, Glud R, Kühl Muyzer G (2007) Diversity of phototropic bacteria in microbial mats from Arctic hot springs (Greenland). Environ Microbiol 9:26–38.  https://doi.org/10.1111/j.1462-2920.2006.01103.x CrossRefPubMedGoogle Scholar
  80. Rowland JG, Pang X, Suzuki I, Murata N, Simon WJ, Slabas AR (2010) Identification of components associated with thermal acclimation of photosystem II in Synechocystis sp. PLoS One 5(5):e10511.  https://doi.org/10.1371/journal.pone.0010511 CrossRefPubMedPubMedCentralGoogle Scholar
  81. Sánchez-Baracaldo P (2015) Origin of marine planktonic cyanobacteria. Sci Rep 5:17418.  https://doi.org/10.1038/srep17418 CrossRefPubMedPubMedCentralGoogle Scholar
  82. Sano EB, Wall CA, Hutchins PR, Miller SR (2018) Ancient balancing selection on heterocyst function in a cosmopolitan cyanobacterium. Nat Ecol Evol 2:510–519.  https://doi.org/10.1038/s41559-017-0435-9 CrossRefPubMedGoogle Scholar
  83. Schirmer T, Bode W, Huber R, Sidler W, Zuber H (1985) X-ray crystallographic structure of the light-harvesting biliprotein C-phycocyanin from the thermophilic cyanobacterium Mastigocladus laminosus and its resemblance to globin structures. J Mol Biol 184(2):257–277.  https://doi.org/10.1016/0022-2836(85)90379-1 CrossRefPubMedGoogle Scholar
  84. Schwabe H (1837) Über die Algen der Karlsbader warmen Quellen. Linnaea 11:109–127Google Scholar
  85. Schwabe GH (1960) Über den thermobionten kosmopolitan Mastigocladus laminosus Cohn. Blaualgen und Lebensraum V. Schweiz Z Hydrol 22:757–792Google Scholar
  86. Shih PM, Wu D, Latifi A, Axen SD, Fewer DP, Talla E, Calteau A, Cai F, Tandeau de Marsac N, Rippka R, Herdman M, Sivonen K, Coursin T, Laurent T, Goodwin L, Nolan M, Davenport KW, Han CS, Rubin EM, Eisen JA, Woyke T, Gugger M, Kerfeld CA (2013) Improving the coverage of the cyanobacterial phylum using diversity-driven genome sequencing. Proc Natl Acad Sci USA 110:1053–1058.  https://doi.org/10.1073/pnas.1217107110 CrossRefPubMedGoogle Scholar
  87. Singh RN, Tiwari DN (1969) Induction by ultraviolet irradiation of mutation in the blue-green alga Nostoc linckia (Roth) Born. et Flah. Nature 221:62–64.  https://doi.org/10.1038/221062a0 CrossRefPubMedGoogle Scholar
  88. Singh AK, Summer TC, Hong W, Sherman LA (2006) The heat shock response in the cyanobacterium Synechocystis sp. Strain PCC 6803 and regulation of gene expression by HrcA and SigB. Arch Microbiol 186:273–286.  https://doi.org/10.1007/s00203-006-0138-0 CrossRefPubMedGoogle Scholar
  89. Soe K, Yokohama A, Yokohama J, Hara Y (2011) Morphological and genetic diversity of the thermophilic cyanobacterium, Mastigocladus laminosus (Stigonematales, Cyanobacteria) from Japan and Myanmar. Phycol Res 59:135–142.  https://doi.org/10.1111/j.1440-1835.2011.00611.x CrossRefGoogle Scholar
  90. Stal LJ (2017) The effect of oxygen concentration and temperature on nitrogenase activity in the heterocystous cyanobacterium Fischerella sp. Sci Rep 7(1):5402.  https://doi.org/10.1038/s41598-017-05715-0 CrossRefPubMedPubMedCentralGoogle Scholar
  91. Stevens SE, Nierzwicki-Bauer SA, Balkwill DL (1985) Effect of nitrogen starvation on the morphology and ultrastructure of the cyanobacterium Mastigocladus laminosus. J Bacteriol 161(3):1215–1218PubMedPubMedCentralGoogle Scholar
  92. Stewart WD (1970) Nitrogen fixation by blue–green algae in Yellowstone thermal areas. Phycologia 9(3):261–268.  https://doi.org/10.2216/i0031-8884-9-3-261.1 CrossRefGoogle Scholar
  93. Stewart WDP, Haystead A, Pearson HW (1969) Nitrogenase activity in heterocysts of blue–green algae. Nature 224(5216):226.  https://doi.org/10.1038/224226a0 CrossRefPubMedGoogle Scholar
  94. Stucken K, John U, Cembella A, Murillo AA, Soto-Liebe K, Fuentes-Valdés JJ, Friedel M, Plominsky AM, Vásquez M, Glöckner G (2010) The smallest known genomes of multicellular and toxic cyanobacteria: comparison, minimal gene sets for linked traits and the evolutionary implications. PLoS One 5(2):e9235.  https://doi.org/10.1371/journal.pone.0009235 CrossRefPubMedPubMedCentralGoogle Scholar
  95. Suzuki I, Simon WJ, Slabas AR (2006) The heat shock response of Synechocystis sp. PCC 6803 analysed by transcriptomics and proteomics. J Exp Bot 57(7):1573–1578.  https://doi.org/10.1093/jxb/erj148 CrossRefPubMedGoogle Scholar
  96. Thiel V, Hügler M, Ward DM, Bryant DA (2017) The dark side of the Mushroom Spring microbial mat: life in the shadow of chlorophototrophs. II Metabolic functions of abundant community members predicted from metagenomic analyses. Front Microbiol 8:943CrossRefPubMedPubMedCentralGoogle Scholar
  97. Wall CA, Koniges GJ, Miller SR (2014) Divergence with gene flow in a population of thermophilic bacteria: a potential role for spatially varying selection. Mol Ecol 23(14):3371–3383.  https://doi.org/10.1111/mec.12812 CrossRefPubMedGoogle Scholar
  98. Walsby AE (2007) Cyanobacterial heterocysts: terminal pores proposed as sites of gas exchange. Trends Microbiol 15(8):340–349.  https://doi.org/10.1016/j.tim.2007.06.007 CrossRefPubMedGoogle Scholar
  99. Walter JM, Coutinho FH, Dutilh BE, Swings J, Thompson FL, Thompson CC (2017) Ecogenomics and taxonomy of cyanobacteria phylum. Front Microbiol 8:2132.  https://doi.org/10.3389/fmicb.2017.02132 CrossRefPubMedPubMedCentralGoogle Scholar
  100. Ward D, Ferris M, Nold S, Bateson M (1998) A natural view of microbial biodiversity within Hot Spring cyanobacterial mat communities. Microbiol Mol Biol Rev 62:1353–1370PubMedPubMedCentralGoogle Scholar
  101. Watanabe M, Ikeuchi M (2013) Phycobilisome: architecture of a light-harvesting supercomplex. Photosynth Res 116(2–3):265–276.  https://doi.org/10.1007/s11120-013-9905-3 CrossRefPubMedGoogle Scholar
  102. Weissman JC, Radway JC, Wilde EW, Benemann JR (1998) Growth and production of thermophilic cyanobacteria in a simulated thermal mitigation process. Bioresour Technol 65(1–2):87–95.  https://doi.org/10.1016/S0960-8524(98)00008-X CrossRefGoogle Scholar
  103. Whitelegge JP, Zhang H, Aguilera R, Taylor RM, Cramer WA (2002) Full subunit coverage liquid chromatography electrospray ionization mass spectrometry (LCMS+) of an oligomeric membrane protein. Mol Cell Proteom 1(10):816–827.  https://doi.org/10.1074/mcp.M200045-MCP200 CrossRefGoogle Scholar
  104. Whitton B, Potts M (2002) Introduction to the Cyanobacteria. In: Whitton M, Potts B (eds) The ecology of cyanobacteria: their diversity in time and space. Kluwer Academic Publishers, Dordrecht, pp 1–11CrossRefGoogle Scholar
  105. Wickstrom C (1980) Distribution and physiological determinants of blue-green algal nitrogen fixation along a thermogradient. J Phycol 16:436–443.  https://doi.org/10.1111/j.1529-8817.1980.tb03058.x CrossRefGoogle Scholar
  106. Wolk CP, Ernst A, Elhai J (1994) Heterocyst metabolism and development. In: Bryant D (ed) The molecular biology of cyanobacteria. Springer, Dordrecht, pp 769–823CrossRefGoogle Scholar
  107. Yamashita T, Butler WL (1968) Inhibition of chloroplasts by UV-irradiation and heat-treatment. Plant Physiol 43(12):2037–2040.  https://doi.org/10.1104/pp.43.12.2037 CrossRefPubMedPubMedCentralGoogle Scholar
  108. Zhao J, Brand J (1989) Specific bleaching of phycobiliproteins from cyanobacteria and red algae at high temperature in vivo. Arch Microbiol 152:447–452.  https://doi.org/10.1007/BF00446927 CrossRefGoogle Scholar

Copyright information

© Springer Japan KK, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Molecular Genetics and MicrobiologyPontifical Catholic University of ChileSantiagoChile
  2. 2.Department of Life ScienceImperial CollegeLondonUK
  3. 3.Department of OceanographyUniversity of ConcepcionConcepciónChile
  4. 4.Center for Climate and Resilience Research (CR)2SantiagoChile
  5. 5.Physics DepartmentFreie Universität BerlinBerlinGermany

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