Importance of Cyanobacterial Taxonomy in Biotechnological Applications

  • Suvendra Nath Bagchi
  • Prashant Singh


Cyanobacteria possess a host of proteases which unlike heterotrophs do not take part in protein nutrition. Instead, they maintain homeostasis of several vital functions, namely photosynthesis, nitrogen fixation, cellular assembly and disintegration, stress acclimation, and defense against predators. Herein, we review the Clp, FtsH, Deg/HtrA, Ctp, and SppA proteases, which under regular and photooxidative stress conditions maintain the integrity of photosynthetic and cytoplasmic membranes, periplasmic proteins, and photosystem particles, including the core complex protein, D1. The HetR protease by coordinating with the Alr3815 protease enables heterocyte differentiation and protection of nitrogenase from oxygen stress. The cell aggregation PteB proteases and caspases regulate the biomass density of cyanobacterial assemblages, and cyanophycinase mobilizes the reserve N, cyanophycin. Macrocyclization proteases mature up the ribosomally synthesized cyclic peptides of cyanobactin class with varied bioactivities. Numerous cyano-proteases listed in the UniProt database are homologues of eubacteria and higher plants with mostly unknown functions but with immense evolutionary significance in understanding the gene flow across bacteria and chloroplasts. Proteases are exclusive and therefore can be tailor-made to customize peptide drug synthesis and to formulate food additives and antimalarial, antivirulence, and antithrombotic agents. Notwithstanding these opportunities, taxonomic inadequacy and lack of proper nomenclature have adversely affected different biotechnological application processes. As a remedy, we propose that polyphasic approach of classification and reassessment of old taxonomic status may be necessary before patenting/commercialization of biotechnological processes/products.


Chaperon Cyanobacteria Endemism Heterocyte differentiation Photosystem II Phylogenetic analysis Polyphasic approach Protease 



PS thanks the Head, Department of Botany, Banaras Hindu University, Varanasi, for his encouragement and support. PS is grateful to the Department of Science and Technology, Govt. of India, New Delhi, for the sanction of project (No. YSS/2014/000879).


  1. Aguilera A, Berrendero E, Kaštovský J, Echenique RO, Salerno GL (2018) The polyphasic analysis of two native Raphidiopsis isolates supports the unification of the genera Raphidiopsis and Cylindrospermopsis (Nostocales, Cyanobacteria). Phycologia 57:130–146CrossRefGoogle Scholar
  2. Anagnostidis K, Komárek J (1985) Modern approach to the classification system of the cyanophytes 1. Introduction. Algol Stud 38/39:291–302Google Scholar
  3. Anagnostidis K & Komárek J (1988). Modern approach to the classification system of the cyanophytes 3. Oscillatoriales Algol Stud 50/53: 327–472Google Scholar
  4. Anagnostidis K, Komárek J (1990) Modern approach to the classification system of the cyanophytes 5. Stigonematales Algol Stud 86:1–74Google Scholar
  5. Andersson FI, Tryggvesson A, Sharon M, Diemand AV, Classen M, Best C, Schmidt R, Schelin J, Stanne TM, Bukau B, Robinson CV, Witt S, Mogk A, Clarke AK (2009) Structure and function of a novel type of ATP-dependent Clp protease. J Biol Chem 284:13519–13532PubMedPubMedCentralCrossRefGoogle Scholar
  6. Argueta C, Yuksek K, Patel R, Summers ML (2006) Identification of Nostoc punctiforme akinete-expressed genes using differential display. Mol Microbiol 61:748–757PubMedCrossRefGoogle Scholar
  7. Badger MR, Price GD, Long BM, Woodger FJ (2006) The environmental plasticity and ecological genomics of the cyanobacterial CO2 concentrating mechanisms. J Exp Bot 57:249–265PubMedCrossRefGoogle Scholar
  8. 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 67:3329–3338PubMedCrossRefGoogle Scholar
  9. Baier K, Nicklisch S, Lockau W (1996) Evidence for propeptide assisted folding of the calcium-dependent protease of the cyanobacterium Anabaena. Eur J Biochem 241:750–755PubMedCrossRefGoogle Scholar
  10. Baier A, Winkler W, Korte T, Lockau W, Karradt A (2014) Degradation of phycobilisomes in Synechocystis sp. PCC6803: evidence for essential formation of an NblA1/NblA2 heterodimer and its codegradation by a Clp protease complex. J Biol Chem 289:11755–11766PubMedPubMedCentralCrossRefGoogle Scholar
  11. Banerjee S, Prasanna R, Bagchi SN (2013) Purification and characterization of a fibrino(geno)lytic protease from cultured natural isolate of a cyanobacterium, Anabaena fertilissima. J Appl Phycol 25:1111–1122CrossRefGoogle Scholar
  12. Bečková M, Yu J, Krynická V, Kojlo A, Shao S, Konik P, Komenda J, Murray JW, Nixon PJ (2017) Structure of Psb29/Thf1 and its association with the FtsH protease complex involved in photosystem II repair in cyanobacteria. Phil Trans R Soc B 372:20160394. CrossRefGoogle Scholar
  13. Berrendero E, Perona E, Mateo P (2008) Genetic and morphological characterization of Rivularia and Calothrix (Nostocales, Cyanobacteria) from running water. Int J Syst Evol Microbiol 58:447–460PubMedCrossRefGoogle Scholar
  14. Berrendero E, Johansen JR, Kaštovský J, Bohunická M, Čapková K (2016) Macrochaete gen. nov. (Nostocales, Cyanobacteria), a taxon morphologically and molecularly distinct from Calothrix. J Phycol 52:638–655CrossRefGoogle Scholar
  15. Bhaya D, Schwarz R, Grossman AR (2000) Molecular responses to environmental stress. In: Whitton BA, Potts M (eds) The ecology of cyanobacteria. Kluwer Academic, Dordrecht, pp 397–442Google Scholar
  16. Boehm M, Yu J, Krynicka Y, Barker M, Tichy M, Komenda J, Nixon PJ, Nield J (2012) Subunit organization of a Synechocystis hetero-oligomeric thylakoid FtsH complex involved in photosystem II repair. Plant Cell 24:3669–3683PubMedPubMedCentralCrossRefGoogle Scholar
  17. Bohunická M, Pietrasiak N, Johansen JR, Berrendero Gómez E, Hauer T, Gaysina LA, Lukešová A (2015) Roholtiella, gen. nov. (Nostocales, Cyanobacteria)- a tapering and branching cyanobacteria of the family Nostocaceae. Phytotaxa 197:84–103CrossRefGoogle Scholar
  18. Bornet E, Flahault C (1886) Revision des Nostocacées hétérocystées contenues dans les principaux herbiers de France. Ann des Sci Nat Bot 1886; Ser 3:323–81; 4:343-373; 5:51-129; 7:177-262Google Scholar
  19. Bourrelly P (1970) Les alguesd’eaudouce III. Boubée & Cie, ParisGoogle Scholar
  20. Büdel B, Kauff F (2012) Blue-green algae. In: Frey W (ed) Syllabus of plant families, Engler’s syllabus der Pflanzenfamilien, part VI. Borntraeger, Stuttgart, pp 5–39Google Scholar
  21. Casamatta DA, Johansen JR, Vis ML, Broadwater ST (2005) Molecular and morphological characterization of ten polar and near-polar strains within the Oscillatoriales (Cyanobacteria). J Phycol 41:421–438CrossRefGoogle Scholar
  22. Castenholz RW (1992) Species usage, concept, and evolution in the cyanobacteria (blue-green algae). J Phycol 28:737–745CrossRefGoogle Scholar
  23. Castenholz RW (2001) Phylum BX. Cyanobacteria, oxygenic photosynthetic bacteria. In: Boone DR, Castenholz RW (eds) Bergey’s manual of systematic bacteriology, vol 1. Springer-Verlag, New York/Berlin/Heidelberg, pp 473–597CrossRefGoogle Scholar
  24. Cheregi O, Wagner R, Funk C (2016) Insights into the cyanobacterial Deg/HtrA proteases. Front Plant Sci 7.
  25. Dong Y, Huang X, Wu XY, Zhao J (2000) Identification of the active site of HetR protease and its requirement for heterocyst differentiation in the cyanobacterium Anabaena sp. strain PCC 7120. J Bacteriol 182:1575–1579PubMedPubMedCentralCrossRefGoogle Scholar
  26. Driscoll CB, Meyer KA, Šulčius S, Brown NM, Dick GJ, Cao H, Gasiūnas G, Timinskas A, Yin Y, Landry ZC, Otten TG, Davis TW, Watson SB, Dreher TW (2018) A closely-related clade of globally distributed bloom-forming cyanobacteria within the Nostocales. Harm Algae 77:93–107CrossRefGoogle Scholar
  27. Drouet F (1981) Revision of the Stigonemataceae with a summary of the classification of the blue-green algae. Beih Nova Hedwigia 66:1–221Google Scholar
  28. Dubey N, Singh P, Bagchi SN (2018) A calcium-stimulated serine peptidase from a true-branching cyanobacterium, Westiellopsis ramosa sp. nov. Physiol Mol Biol Plants 24:261–273PubMedPubMedCentralCrossRefGoogle Scholar
  29. Dvořák P, Casamatta DA, Hašler P, Jahodářová E, AR & N, Poulíčková A (2017) Diversity of the cyanobacteria. In: Hallenbeck PC (ed) Modern topics in the phototrophic prokaryotes. Springer International Publishing, Cham, pp 3–46CrossRefGoogle Scholar
  30. Elenkin AA (1938) Monographia algarum cyanophycearum aquidulcium et terrestrium in finibus URSS inventarum. (Sinezelenye vodorosli SSSR). Pars spec. (1-2). pp. 1-1908. Moskva-Leningrad: Izd. AN SSSRGoogle Scholar
  31. Fernández-Martínez MA, Ríos ADL, Sancho LG, Pérez-Ortega S (2013) Diversity of endosymbiotic Nostoc in Gunnera magellanica (L) from Tierra del Fuego, Chile. Microb Ecol 66:335–350PubMedCrossRefGoogle Scholar
  32. Flores E, Picossi S, Valladares A, Herrero A (2018) Transcriptional regulation of development in heterocyst-forming cyanobacteria. Biochim Biophys Acta (In press) doi: CrossRefGoogle Scholar
  33. Frémy P (1929) Les Nostocacées de la Normandie. Not Mem Doc Soc Agric Archéol Hist nat Manche 41:197–228Google Scholar
  34. Frias JE, Flores E, Herrero A (1994) Requirement of the regulatory protein NtcA for the expression of nitrogen assimilation and heterocyst development genes in the cyanobacterium Anabaena sp. PCC 7120. J Molec Microbiol 14:823–832CrossRefGoogle Scholar
  35. Funk C, Hauβühl K, Adamska I (2001) Family of Deg/Htr proteases in the cyanobacterium Synechocystis sp. PCC6803: Investigations toward their expression and function. In Larkum T, Critchley C (eds.) CSIRO Publishing, Brisbane, AustraliaGoogle Scholar
  36. Garcia-Pichel F, Cortes AL, Nübel U (2001) Phylogenetic and morphological diversity of cyanobacteria in soil desert crusts from the Colorado plateau. Appl Environ Microbiol 67:1902–1910PubMedPubMedCentralCrossRefGoogle Scholar
  37. Geitler L (1925) Cyanophyceae. In: Pascher A (ed.) Süswasserflora Gustav Fischer Verl., Jena, 12: 481Google Scholar
  38. Geitler L (1932) Cyanophyceae. – In: Rabenhorst L (ed.) Kryptogamen–Flora von Deutschland, Österreich und der Schweiz. Akademische Verlagsgesellschaft, Leipzig, Germany, pp. 673–1056Google Scholar
  39. Geitler L (1942) Schizophyta (Klasse Schizophyceae). In: Engler A, Prantl K (eds.) Natürliche Pflanzenfamilien Duncker & Humblot, Berlin 1942;1b:1–232Google Scholar
  40. Genuário DB, Vaz GMV, Hentschke GS, Anna CLS, Fiore MF (2015) Halotia gen. nov., a phylogenetically and physiologically coherent cyanobacterial genus isolated from marine coastal environments. Int J Syst Evol Microbiol 65:663–675PubMedCrossRefGoogle Scholar
  41. Giovannoni SJ, Turner S, Olsen GJ, Barns S, Lane DJ, Pace NR (1988) Evolutionary relationships among cyanobacteria and green chloroplasts. J Bacteriol 170:3584–3592PubMedPubMedCentralCrossRefGoogle Scholar
  42. Halinen K, Fewer DP, Sivonen LM, Lyra C, Eronen E, Sivonen K (2008) Genetic diversity in strains of the genus Anabaena isolated from planktonic and benthic habitats of the Gulf of Finland (Baltic Sea). FEMS Microbiol Ecol 64:199–208PubMedCrossRefGoogle Scholar
  43. Hall M, Wagner R, Lam XT, Funk C, Persson K (2017) The HhoA protease from Synechocystis sp. PCC 6803 – novel insights into structure and activity regulation. J Str Biol 198:147–153CrossRefGoogle Scholar
  44. Halperin T, Ostersetzer O, Adam Z (2001) ATP – dependent association between subunits of Clp protease in pea chloroplasts. Planta 213:614–619PubMedCrossRefGoogle Scholar
  45. Hauer T, Bohunická M, Johansen JR, Mareš J, Berrendero-Gomez E (2014) Reassessment of the cyanobacterial family Microchaetaceae and establishment of new families Tolypothrichaceae and Godleyaceae. J Phycol 50:1089–1100PubMedCrossRefGoogle Scholar
  46. Henson BJ, Hesselbrock SM, Watson LE, Barnum SR (2004) Molecular phylogeny of the heterocystous cyanobacteria (subsections IV and V) based on nifD. Int J Syst Evol Microbiol 54:493–497PubMedCrossRefGoogle Scholar
  47. Hrouzek P, Ventura S, Lukešová A, Mugnai MA, Turicchia S, Komárek J (2005) Diversity of soil Nostoc strains: phylogenetic and phenotypic variability. Algol Stud 117:16–122CrossRefGoogle Scholar
  48. Hrouzek P, Lukešová A, Mareš J, Ventura S (2013) Description of the cyanobacterial genus Desmonostoc gen. nov. including D. muscorum comb. nov. as a distinct, phylogenetically coherent taxon related to the genus Nostoc. Fottea 13:201–213CrossRefGoogle Scholar
  49. Imai K, Kitayama Y, Kondo T (2013) Elucidation of the role of Clp protease components in circadian rhythm by genetic deletion and overexpression in cyanobacteria. J Bactriol 195:4517–4526CrossRefGoogle Scholar
  50. Kabirnataj S, Nematzadeh GA, Talebi AF, Tabatabaei M, Singh P (2018) Neowestiellopsis gen. nov, a new genus of true branched cyanobacteria with the description of Neowestiellopsis persica sp. nov. and Neowestiellopsis bilateralis sp. nov., isolated from Iran. Plant Syst Evol 304:501–510CrossRefGoogle Scholar
  51. Karnauchov I, Herrmann RG, Pakrasi HB, Klösgen RB (1997) Transport of CtpA protein from the cyanobacterium Synechocystis 6803 across the thylakoid membrane in chloroplasts. Eur J Biochem 249:497–504PubMedCrossRefGoogle Scholar
  52. Klemenčič M, Funk C (2018) Structural and functional diversity of caspase homologues in non-metazoan organisms. Protoplasma 255:387–397PubMedCrossRefGoogle Scholar
  53. Klemenčič M, Novinec M, Dolinar M (2015) Orthocaspases are proteolytically active prokaryotic caspase homologues: the case of Microcystis aeruginosa. Molec Microbiol 98:142–150CrossRefGoogle Scholar
  54. Knappe TA, Manzenrieder F, Mas-Moruno C, Linne U, Sasse F, Kessler H, Xie X, Marahiel MA (2011) Introducing lasso peptides as molecular scaffolds for drug design: engineering of an integrin antagonist. Angew Chem Int Ed 50:8714–8717CrossRefGoogle Scholar
  55. Komárek J (2005) Studies on the cyanophytes (Cyanobacteria, cyanoprokaryota) of Cuba 11. Freshwater Anabaena species. Preslia 77:211–234Google Scholar
  56. Komárek J (2008) The cyanobacterial genus Macrospermum. Fottea 8:79–86CrossRefGoogle Scholar
  57. Komárek J (2010) Modern taxonomic revision of planktic-nostocacean cyanobacteria: a short review of genera. Hydrobiology 639:231–243CrossRefGoogle Scholar
  58. Komárek J (2013) Cyanoprokaryota. 3. Heterocytous genera. In: Büdel B, Gärtner G, Krienitz L, Schagerl M (eds) Süswasserflora von Mitteleuropa/Freshwater flora of Central Europe. Springer Spektrum Berlin, Heidelberg, p 1130Google Scholar
  59. Komárek J (2016) A polyphasic approach for the taxonomy of cyanobacteria: principles and applications. Eur J Phycol 51:346–353CrossRefGoogle Scholar
  60. Komárek J (2018) Several problems of the polyphasic approach in the modern cyanobacterial system. Hydrobiologia 811:7–17CrossRefGoogle Scholar
  61. Komárek J, Anagnostidis K (1986) Modern approach to the classification system of the cyanophytes 2. Chroococcales Algol Stud 43:157–226Google Scholar
  62. Komárek J, Anagnostidis K (1989) Modern approach to the classification system of the cyanophytes 4. Nostocales Algol Stud 56:247–345Google Scholar
  63. Komarek J, Komárková J (2004) Taxonomic review of the cyanoprokaryotic genera Planktothrixand Planktothricoides. Czech Phycol 4:1–18Google Scholar
  64. Komárek J, Zapomělová E (2007) Plankticmorphospecies of the cyanobacterial genus Anabaena = subg. Dolichospermum– 1. Part: coiled types. Fottea 7:1–31CrossRefGoogle Scholar
  65. Komárek J, Zapomělová E (2008) Plankticmorphospecies of the cyanobacterial genus Anabaena = subg. Dolichospermum– 2. Part: straight types. Fottea 8:1–14CrossRefGoogle Scholar
  66. Komárek J, Kaštovský J, Mareš J, Johansen J (2014) Taxonomic classification of cyanoprokaryotes (cyanobacterial genera), using a polyphasic approach. Preslia 86:295–335Google Scholar
  67. Krynická V, Tichý M, Krafl J, Yu J, Kaňa R, Boehm M, Nixon PJ, Komenda J (2014) Two essential FtsH proteases control the level of the Fur repressor during iron deficiency in the cyanobacterium Synechocystis sp.PCC6803. Molec Microbiol 94:609–624CrossRefGoogle Scholar
  68. Kust A, Kozlíková–Zapomělová E, Mareš J, Řeháková K (2015) A detailed morphological, phylogenetic and ecophysiological analysis of four benthic Anabaena (Nostocales, Cyanobacteria) strains confirms deep heterogeneity within the genus. Fottea 15:191–202CrossRefGoogle Scholar
  69. Lam XT, Aigner H, Timmerman E, Gevaert K, Funk C (2015) Proteomic approaches to identify substrates of the three Deg/HtrA proteases of the cyanobacterium Synechocystis sp. PCC 6803. Biochem J 468:373–384CrossRefGoogle Scholar
  70. Law AM, Lai SWS, Tavares J, Kimber MS (2009) The structural basis of beta-peptide-specific cleavage by the serine protease cyanophycinase. J Mol Biol 392:393–404PubMedCrossRefGoogle Scholar
  71. Lee DH, Zo YG, Kim SJ (1996) Non-radioactive method to study genetic profiles of bacterial communities by PCR-single- strand conformation polymorphism. Appl Environ Microbiol 62:3112–3120PubMedPubMedCentralGoogle Scholar
  72. Lee J, McIntosh J, Hathaway BJ, Schmidt EW (2009) Using marine natural products to discover a protease that catalyzes peptide macrocyclization of diverse substrates. J Am Chem Soc 131:2122–2124PubMedPubMedCentralCrossRefGoogle Scholar
  73. Lehtimäki J, Lyra C, Suomalainen S, Sundman P, Rouhiainen L, Paulin L, Salkinoja-Salonen M, Sivonen K (2000) Characterization of Nodulariastrains, cyanobacteria from brackish waters, by genotypic and phenotypic methods. Int J Syst Evol Microbiol 50:1043–1053PubMedCrossRefGoogle Scholar
  74. Leikoski N, Fewer DP, Jokela J, Wahlsten M (2010) Highly diverse cyanobactins in strains of the genus Anabaena. Appl Environ Microbiol 76:701–709PubMedCrossRefGoogle Scholar
  75. León-Tejera H, González-Resendiz L, Johansen JR, Segal-kischinevsky C, Escobar V, Lois LA (2016) Phylogenetic position reevaluation of Kyrtuthrix and description of K. huatulcensis from Mexico’s Pacific coast. Phytotaxa 278(1):18CrossRefGoogle Scholar
  76. Li X, Dreher TW, Li R (2016) An overview of diversity, occurrence, genetics and toxin production of bloom forming Dolichospermum (Anabaena) species. Harm Algae 54:54–68CrossRefGoogle Scholar
  77. Lockau VL, Massalsky B, Dirmair A (1998) Purification and partial characterization of a calcium stimulated protease from the cyanobacterium, Anabaena variabilis. Eur J Biochem 172:433–438CrossRefGoogle Scholar
  78. Lu Z, Sha Z, Tian Y, Zhang X, Liu B, Wu Z (2017) Polyphenolic allelochemical pyrogallic acid induces caspase-3(like)-dependent programmed cell death in the cyanobacterium Microcystis aeruginosa. Algal Res 21:148–155CrossRefGoogle Scholar
  79. Lyra C, Hantula J, Vanio E, Rapal J, Rouhiainen L, Sivonen K (1997) Characterization of cyanobacteria by SDS-PAGE of whole cell proteins and PCR/RFLP of 16S rRNA gene. Arch Microbiol 168:176–184PubMedCrossRefGoogle Scholar
  80. Lyra C, Laamanen M, Lehtimäki JM, Surakka A, Sivonen K (2005) Benthic cyanobacteria of the genus Nodularia are non toxic, without gas vacuoles, able to glide and genetically more diverse than planktonic Nodularia. Int J Syst Evol Microbiol 55:555–568PubMedCrossRefGoogle Scholar
  81. Maldener I, Lockau W, Cai Y, Wolk CP (1991) Calcium-dependent protease of the cyanobacterium Anabaena: molecular cloning and expression of the gene in Escherichia coli, sequencing and site-directed mutagenesis. Mol Gen Genet 225:113–120PubMedCrossRefGoogle Scholar
  82. Mareš J (2010) Anabaena fuscovaginata (Nostocales), a new cyanobacterial species from periphyton of the freshwater alkaline marsh of Everglades, South Florida, USA. Fottea 10:235–243CrossRefGoogle Scholar
  83. Mareš J (2018) Multilocus and SSU rRNA gene phylogenetic analyses of available cyanobacterial genomes, and their relation to the current taxonomic system. Hydrobiologia 811:19–34CrossRefGoogle Scholar
  84. Masuda T, Bernát G, Bečková M, Kotabová E, Lawrenz E, Lukeš M, Komenda J, Prášil O (2018) Diel regulation of photosynthetic activity in the oceanic unicellular diazotrophic cyanobacterium Crocosphaera watsonii WH8501. Environ Microbiol 20:546–556PubMedCrossRefGoogle Scholar
  85. McGregor GB, Sendall BC (2017a) Iningainema pulvinus gen nov., sp nov. (Cyanobacteria, Scytonemataceae) a new nodularin producer from Edgbaston reserve, North-Eastern Australia. Harm Algae 62:10–19CrossRefGoogle Scholar
  86. McGregor GB, Sendall BC (2017b) Ewamianiathermalis gen. et sp. nov. (Cyanobacteria, Scytonemataceae), a new cyanobacterium from Talaroo thermal springs, North-Eastern Australia. Aust Syst Bot 30:38–47CrossRefGoogle Scholar
  87. Mikhailov VA, Ståhlberg F, Clarke AK, Robinson CV (2015) Dual stoichiometry and subunit organization in the ClpP1/P2 protease from the cyanobacterium Synechococcus elongatus. J Str Biol. 192:519–527CrossRefGoogle Scholar
  88. Moten D, Batsalova T, Basheva D, Mladenov R, Dzhambazov B, Teneva I (2018) Outer membrane efflux protein (OMEP) is a suitable molecular marker for resolving the phylogeny and taxonomic status of closely related cyanobacteria. Phycol Res 66:31–36CrossRefGoogle Scholar
  89. Nabout JC, Rocha BS, Carneiro FM, Sant’Anna CL (2013) How many species of Cyanobacteria are there? Using a discovery curve to predict the species number. Biodivers Conserv 22:2907–2918CrossRefGoogle Scholar
  90. Neilan BA, Jacobs D, Goodman AE (1995) Genetic diversity and phylogeny of toxic cyanobacteria determined by DNA polymorphisms within the phycocyanin locus. Appl Environ Microbiol 61:3875–3883PubMedPubMedCentralGoogle Scholar
  91. Neilan BA, Burns BP, Relman DA, Lowe DR (2002) Molecular identification of cyanobacteria associated with stromatolites from distinct geographical locations. Astrobiology 2:271–280PubMedCrossRefGoogle Scholar
  92. Nelissen B, De Baere R, Wilmotte A, DeWatcher R (1996) Phylogenetic relationships of Non axenic filamentous cyanobacterial strains based on 16S rRNA sequence analysis. J Mol Evol 42:194–200PubMedCrossRefGoogle Scholar
  93. Ng CL, Fidock DA, Bogyo M (2017) Protein degradation systems as Antimalarial therapeutic targets. Trends Parasitol 33:731–743PubMedPubMedCentralCrossRefGoogle Scholar
  94. Nishimura K, Kato Y, Sakamoto W (2016) Chloroplast proteases: updates on proteolysis within and across suborganellar compartments. Plant Physiol 171:2280–2293PubMedPubMedCentralGoogle Scholar
  95. Oliveira P, Martins NM, Santos M, Couto NAS (2015) The Anabaena sp. PCC 7120 exoproteome: taking a peek outside the box. Life 5:130–163PubMedPubMedCentralCrossRefGoogle Scholar
  96. Ongpipattanakul C, Nair SK (2018) Biosynthetic proteases that catalyze the macrocyclization of ribosomally synthesized linear peptides. Biochemistry (In press). PubMedCrossRefGoogle Scholar
  97. Oren A, Ventura S (2017) The current status of cyanobacterial nomenclature under the “prokaryotic” and the “botanical” code. Antonie Leeuwenhoek 110:157–169Google Scholar
  98. Otsuka S, Suda S, Shibata S, Oyaizu H, Matsumoto S, Watanabe MM (2001) A proposal for the unification of five species of the cyanobacterial genus Microcystis Kützing ex Lemmermann 1907 under the rules of the Bacteriological Code. Int J Syst Evol Microbiol 51:873–879PubMedCrossRefGoogle Scholar
  99. Oueis E, Nardone B, Jaspars M, Westwood NJ, Naismith NJ (2017a) Synthesis of hybrid cyclopeptides through enzymatic macrocyclization. ChemistryOpen 6:11–14PubMedCrossRefGoogle Scholar
  100. Oueis E, Stevenson H, Jaspars M, Westwood NJ, Naismith JH (2017b) Bypassing the proline/thiazoline requirement of the macrocyclase PatG. Chem Commun 53:12274–12277CrossRefGoogle Scholar
  101. 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 58:553–564PubMedCrossRefGoogle Scholar
  102. Parnasa R, Nagar E, Sendersky E, Reich Z, Simkovsky R, Golden S, Schwarz R (2016) Small secreted proteins enable biofilm development in the cyanobacterium Synechococcus elongatus. Sci Rep 6:32209. CrossRefPubMedPubMedCentralGoogle Scholar
  103. Perkerson RB, Johansen JR, Kováčik L, Brand J, Kaštovský J, Casamatta DA (2011) A unique pseudanabaenalean (Cyanobacteria) genus Nodosilinea gen. nov. based on morphological and molecular data. J Phycol 47:1397–1412CrossRefGoogle Scholar
  104. Pojidaeva ES, Sokolenko AV (2017) In cyanobacteria Synechocystis sp. PCC6803 the light-dependent level of SppA2 protein is regulated by SppA1 peptidase. Russ J Plant Physiol 64:319–324CrossRefGoogle Scholar
  105. Pojidaeva E, Zinchenko V, Shestakov SV, Sokolenko A (2004) Involvement of the SppA1 peptidase in acclimation to saturating light intensities in Synechocystis sp. strain PCC 6803. J Bacteriol 186:3991–3999PubMedPubMedCentralCrossRefGoogle Scholar
  106. Ponndorf D, Ehmke S, Walliser B, Thoss K, Unger C, Görs S, Das G, Metges CC, Broer I, Nausch H (2017) Stable production of cyanophycinase in Nicotiana benthamiana and its functionality to hydrolyse cyanophycin in the murine intestine. Plant Biotechnol J 15:605–613PubMedCrossRefGoogle Scholar
  107. Rajaniemi P, Hrouzek P, Kastovska K, Willame R, Rantala A, Hoffmann L, Komárek J, Sivonen K (2005) Phylogenetic and morphological evaluation of the genera Anabaena, Aphanizomenon, Trichormusand Nostoc (Nostocales, cyanobacteria). Int J Syst Evol Microbiol 55:11–26PubMedCrossRefGoogle Scholar
  108. Ramos V, Morais J, Castelo-Brancol R, Pinheiro Â, Martins J, Regueiras A, Pereira AL, Lopes VR, Frazão B, Gomes D, Moreira C, Costa MS, Brûle S, Faustino S, Martins R, Saker M, Osswald J, Leão PN, Vasconcelos VM (2018) Cyanobacterial diversity held in microbial biological resource centers as a biotechnological asset: the case study of the newly established LEGE culture collection. J Appl Phycol 30:1437–1451PubMedPubMedCentralCrossRefGoogle Scholar
  109. Rasmussen U, Svenning MM (1998) Fingerprinting of cyanobacteria based on PCR with primers derived from short and long tandemly repeated repetitive sequences. Appl Environ Microbiol 64:265–272PubMedPubMedCentralGoogle Scholar
  110. Rathore S, Sinha D, Asad M, Böttcher T, Afrin F, Chauhan VS, Gupta D, Sieber SA, Mohmmed A (2010) A cyanobacterial serine protease of Plasmodium falciparum is targeted to the apicoplast and plays an important role in its growth and development. Mol Microbiol 77:873–890PubMedGoogle Scholar
  111. 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 46:481–502CrossRefGoogle Scholar
  112. Ribeiro KF, Duarte L, Crossetti LO (2018) Everything is not everywhere: a tale on the biogeography of cyanobacteria. Hydrobiologia 820:23–48CrossRefGoogle Scholar
  113. Richter R, Hejazi M, Kraft R, Ziegler K, Lockau W (1999) Cyanophycinase, a peptidase degrading the cyanobacterial reserve material multi-L-arginyl-poly-L-aspartic acid (cyanophycin) – molecular cloning of the gene of Synechocystis sp PCC 6803, expression in Escherichia coli, and biochemical characterization of the purified enzyme. Eur J Biochem 263:163–169PubMedCrossRefGoogle Scholar
  114. Rippka R, Deruelles J, Waterbury J, Herdman M & Stanier RY (1979). Generic assignments, strain histories and properties of pure cultures of cyanobacteria. Microbiology 111:1–61Google Scholar
  115. Rott E, Pentecost A, Mareš A (2018) Introduction: recent developments in cyanobacterial research with special reference to aquatic habitats, molecular ecology and phylogenetic taxonomy. Hydrobiologia 811:1–6CrossRefGoogle Scholar
  116. Rudi K, Skulberg OM, Skulberg R, Jakobsen KS (2000) Application of sequence specific labelled 16S rRNA gene oligo nucleotide probes for genetic profiling of cyanobacterial abundance and diversity by array hybridization. Appl Environ Microbiol 66:4004–4011PubMedPubMedCentralCrossRefGoogle Scholar
  117. Seckbach J, Oren A (2007) Oxygenic photosynthetic microorganisms in extreme environment: possibilities and limitations. In: Seckbach J (ed) Algae and cyanobacteria in extreme environments. Springer, DordrechtCrossRefGoogle Scholar
  118. Selão T, Zhang L, Knoppová J, Komenda J, Norling B (2016) Photosystem II assembly steps take place in the thylakoid membrane of the cyanobacterium Synechocystis sp. PCC6803. Plant Cell Physiol 57:95–104PubMedCrossRefGoogle Scholar
  119. Shalygin S, Shalygina R, Johansen JR, Pietrasiak N, Berrendero Gómez E, Bohunická M, Mareš J, Sheil CA (2017) Cyanomargarita gen. nov. (Nostocales, Cyanobacteria): convergent evolution resulting in a cryptic genus. J Phycol 53:762–777PubMedCrossRefGoogle Scholar
  120. Shao S, Cardona T, Nixon PJ (2018) Early emergence of the FtsH proteases involved in photosystem II repair. Photosynthetica 56:163–177CrossRefGoogle Scholar
  121. Shestakov SV, Anbudurai PR, Stanbekova GE, Gadzhiev A, Lind LK, Pakrasi HB (1994) Molecular cloning and characterization of the ctpA gene encoding a carboxyl-terminal processing peptidase. Analysis of a spontaneous photosystem II-deficient mutant strain of the cyanobacterium Synechocystis sp. PCC 6803. J Biol Chem 269:19354–19359PubMedGoogle Scholar
  122. Shi Y, Zhao W, Zhang W, Zhao J (2006) Regulation of intracellular free calcium concentration during heterocyst differentiation by HetR and NtcA in Anabaena sp. PCC 7120. Proc Natl Acad Sci U S A 103:11334–11339PubMedPubMedCentralCrossRefGoogle Scholar
  123. 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 U S A 110:1053–1058PubMedCrossRefGoogle Scholar
  124. Sihvonen LM, Lyra C, Fewer DP, Rajaniemi-Wacklin P, Lehtimäki JM, Wahlsten M, Sivonen K (2007) Strains of the cyanobacterial genera Calothrix and Rivularia isolated from the Baltic Sea display cryptic diversity and are distantly related to Gloeotrichia and Tolypothrix. FEMS Microbiol Ecol 61:74–84Google Scholar
  125. Silber KR, Keiler KC, Sauer RT (1992) Sp: a tail-specific peptidase that selectively degrades proteins with nonpolar C termini. Proc Natl Acad Sci (USA) 89:295–299PubMedCentralCrossRefPubMedGoogle Scholar
  126. Sivonen K, Leikoski N, Fewer DP, Jokela J (2010) Cyanobactins-ribosomal cyclic peptides produced by cyanobacteria. Appl Microbiol Biotechnol 86:1213–1225PubMedPubMedCentralCrossRefGoogle Scholar
  127. Skácelová O, Zapomělová E (2010) Remarks on the occurrence and ecology of several interesting cyanobacterial morphospecies found in South Moravian wetlands. Acta Musei Moraviae, Scientiae Iologicae 95:201–221Google Scholar
  128. Stanier RY, van Niel CB (1962) The concept of a bacterium. Arch Mikrobiol 42:17–35PubMedCrossRefGoogle Scholar
  129. Stanne TM, Pojidaeva E, Andersson FI, Clarke AK (2007) Distinctive types of ATP-dependent Clp proteases in cyanobacteria. J Biol Chem 282:14394–14402PubMedCrossRefGoogle Scholar
  130. Starmach K (1966) Cyanophyta-Sinice. In Flora slodkowodna Polski. 2. (eds) Warszawa: PAN, Panstwowe Wydawnictwo Naukowe, pp. 753Google Scholar
  131. Strohmeier U, Gerdes C, Lockau W (1994) Proteolysis in heterocyst forming cyanobacteria: characterization of a further enzyme with trypsin-like specificity, and of a prolyl endopeptidase from Anabaena variabilis. Z Naturforsch 49:70–78CrossRefGoogle Scholar
  132. Stuart RK, Mayali X, Lee JZ, Everroad RC, Hwang M, Bebout BM, Weber PK, Pett-Ridge J, Thelen MP (2016) Cyanobacterial reuse of extracellular organic carbon in microbial mats. ISME J 10:1240–1251PubMedCrossRefGoogle Scholar
  133. Suda S, Watanabe MM, Otsuka S, Mahakahant A, Yongmanitchai W, Nopartnaraporn N, Liu Y, Day JG (2002) Taxonomic revision of water bloom-forming species of oscillatorioid cyanobacteria. Int J Syst Evol Microbiol 52:1577–1595PubMedGoogle Scholar
  134. Suradkar A, Villanueva C, Gaysina LA, Casamatta DA, Saraf A, Dighe G, Mergu R, Singh P (2017) Nostoc thermotolerans sp. nov., a soil-dwelling species of Nostoc (Cyanobacteria). Int J Syst Evol Microbiol 67:1296–1305PubMedCrossRefGoogle Scholar
  135. Thomazeau S, Houdan-Fourmont A, Couté A, Duval C, Couloux A, Rousseau F, Bernard C (2010) The contribution of Sub-Saharan African strains to the phylogeny of cyanobacteria: focusing on the Nostocaceae (Nostocales). J Phycol 46:564–579CrossRefGoogle Scholar
  136. Turner S (1997) Molecular systematic of oxygenic photosynthetic bacteria. Plant Syst Evol 11:13–52CrossRefGoogle Scholar
  137. Urbach E, Robertson DL, Chisholm SW (1992) Multiple evolutionary origins of prochlorophytes within the cyanobacterial radiation. Nature (London) 355:267–270CrossRefGoogle Scholar
  138. Vaccarino MA, Johansen JR (2011) Scytonema topsiscontorta sp. nov. (Nostocales), a new species from the Hawaiian Islands. Fottea 11:149–161CrossRefGoogle Scholar
  139. Valladares A, Flores E, Herrero A (2016) The heterocyst differentiation transcriptional regulator HetR of the filamentous cyanobacterium Anabaena forms tetramers and can be regulated by phosphorylation. Molec Microbiol 99:808–819CrossRefGoogle Scholar
  140. Versalovic J, Schneider M, de Bruijn FJ, Lupski JR (1994) Genomic fingerprinting of bacteria using repetitive sequence based PCR (rep-PCR). Methods Cell Biol 5:25–40Google Scholar
  141. Vilhauer L, Jervis J, Ray WK, Helm RF (2014) The exo-proteome and exo-metabolome of Nostoc punctiforme (cyanobacteria) in the presence and absence of nitrate. Arch Microbiol 196:357–367PubMedCrossRefGoogle Scholar
  142. Wacklin P, Hoffmann L, Komárek J (2009) Nomenclatural validation of the genetically revised cyanobacterial genus Dolichospermum (Ralfs ex Bornetet Flahault) comb. Nova. Fottea 9:59–64CrossRefGoogle Scholar
  143. Wilmotte A (1994) Molecular evolution and taxonomy of the cyanobacteria. In: Bryant A (ed) The molecular biology of cyanobacteria. Kluwer Academic Publishers, Dordrecht, pp 1–25Google Scholar
  144. Yada E, Nagata H, Noguchi Y, Kodera Y, Nishimura H, Inada Y, Matsushima A (2005) An arginine specific protease from Spirulina platensis. Mar Biotechnol 7:474–480PubMedCrossRefGoogle Scholar
  145. Yang GH, Hu B, Zhao JD (2011) Specific degradation of photosystem II D1 protein by a protease (Alr3815) in heterocysts of the cyanobacterium Anabaena sp. PCC7120. Chin Sci Bull 56:1068. CrossRefGoogle Scholar
  146. Yu AY, Houry WA (2007) ClpP: a distinctive family of cylindrical energy- dependent serine proteases. FEBS Lett 581:3749–3757PubMedCrossRefGoogle Scholar
  147. Zak E, Norling B, Maitra R, Huang F, Andersson B, Pakrasi HB (2001) The initial steps of biogenesis of cyanobacterial photosystems occur in plasma membranes. Proc Natl Acad Sci U S A 98:13443–13448PubMedPubMedCentralCrossRefGoogle Scholar
  148. Zapomělová E, Jezberová J, Hrouzek P, Hisem D, Řeháková K, Komárková J (2009) Polyphasic characterization of three strains of Anabaena reniformis and Aphanizomenon aphanizomenoides (cyanobacteria) and their re–classification to Sphaerospermum gen. nov. (incl. Anabaena kisseleviana). J Phycol 45:1363–1373PubMedCrossRefGoogle Scholar
  149. Zapomělová E, Hrouzek P, Řezanka T, Jezberová J, Řeháková K, Hisem D, Komárková J (2011) Polyphasic characterization of Dolichospermum spp. and Sphaerospermopsis spp. (Nostocales, Cyanobacteria): morphology, 16S rRNA gene sequences and fatty acid and secondary metabolite profiles. J Phycol 47:1152–1163PubMedCrossRefGoogle Scholar
  150. Zapomělová E, Skácelová O, Pumann P, Kopp R, Janeček E (2012) Biogeographically interesting planktonic Nostocales (Cyanobacteria) in the Czech Republic and their polyphasic evaluation resulting in taxonomic revisions of Anabaena bergii Ostenfeld 1908 (Chrysosporumgen. nov.) and A. tenericaulis Nygaard 1949 (Dolichospermum tenericaulecomb. nova). Hydrobiologia 698:353–365CrossRefGoogle Scholar
  151. Zapomělová EK, Ferrari G, Pérez MDC (2016) Dolichospermum uruguayense sp. nov., a planktic nostocacean cyanobacterium from the Lower Uruguay River, South America. Fottea 16:189–200CrossRefGoogle Scholar
  152. Zehr JP, Mellon MT, Hiorns WD (1997) Phylogeny of cyanobacterial nifH genes: evolutionary implications and potential applications to natural assemblages. Microbiology 143:1443–1450PubMedCrossRefGoogle Scholar
  153. Zienkiewicz M, Ferenc A, Wasilewska W, Romanowska E (2012) High light stimulates Deg1-dependent cleavage of the minor LHCII antenna proteins CP26 and CP29 and the PsbS protein in Arabidopsis thaliana. Planta 235:279–288PubMedCrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  • Suvendra Nath Bagchi
    • 1
  • Prashant Singh
    • 2
  1. 1.Department of Biological ScienceRani Durgavati UniversityJabalpurIndia
  2. 2.Department of BotanyBanaras Hindu UniversityVaranasiIndia

Personalised recommendations