While photosynthetic processes have become increasingly understood in cyanobacterial model strains, differences in the spatial distribution of thylakoid membranes among various lineages have been largely unexplored. Cyanobacterial cells exhibit an intriguing diversity in thylakoid arrangements, ranging from simple parietal to radial, coiled, parallel, and special types. Although metabolic background of their variability remains unknown, it has been suggested that thylakoid patterns are stable in certain phylogenetic clades. For decades, thylakoid arrangements have been used in cyanobacterial classification as one of the crucial characters for definition of taxa. The last comprehensive study addressing their evolutionary history in cyanobacteria was published 15 years ago. Since then both DNA sequence and electron microscopy data have grown rapidly. In the current study, we map ultrastructural data of >200 strains onto the SSU rRNA gene tree, and the resulting phylogeny is compared to a phylogenomic tree. Changes in thylakoid architecture in general follow the phylogeny of housekeeping loci. Parietal arrangement is resolved as the original thylakoid organization, evolving into complex arrangement in the most derived group of heterocytous cyanobacteria. Cyanobacteria occupying intermediate phylogenetic positions (greater filamentous, coccoid, and baeocytous types) exhibit fascicular, radial, and parallel arrangements, partly tracing the reconstructed course of phylogenetic branching. Contrary to previous studies, taxonomic value of thylakoid morphology seems very limited. Only special cases such as thylakoid absence or the parallel arrangement could be used as taxonomically informative apomorphies. The phylogenetic trees provide evidence of both paraphyly and reversion from more derived architectures in the simple parietal thylakoid pattern. Repeated convergent evolution is suggested for the radial and fascicular architectures. Moreover, thylakoid arrangement is constrained by cell size, excluding the occurrence of complex architectures in cyanobacteria smaller than 2 μm in width. It may further be dependent on unknown (eco)physiological factors as suggested by recurrence of the radial type in unrelated but morphologically similar cyanobacteria, and occurrence of special features throughout the phylogeny. No straightforward phylogenetic congruences have been found between proteins involved in photosynthesis and thylakoid formation, and the thylakoid patterns. Remarkably, several postulated thylakoid biogenesis factors are partly or completely missing in cyanobacteria, challenging their proposed essential roles.

Center Algatech Institute of Microbiology Czech Academy of Sciences Třeboň Czechia

Department of Aquatic Microbial Ecology Institute of Hydrobiology Biology Centre Czech Academy of Sciences České Budějovice Czechia

Faculty of Science University of South Bohemia České Budějovice Czechia

Institute of Aquaculture Faculty of Fisheries and Protection of Waters University of South Bohemia České Budějovice Czechia

Laboratory of Molecular Genetics of Bacteria Institute of Microbiology Czech Academy of Sciences Prague Czechia

Zobrazit více v PubMed

Alvarenga D. O., Andreote A. P. D., Branco L. H. Z., Fiore M. F. (2017). Kryptousia macronema gen. nov., sp. nov. and Kryptousia microlepis sp. nov., nostocalean cyanobacteria isolated from phyllospheres. Int. J. Syst. Evol. Microbiol. 67 3301–3309. 10.1099/ijsem.0.002109 PubMed DOI

Alvarenga D. O., Rigonato J., Branco L. H. Z., Melo I. S., Fiore M. F. (2016). Phyllonema aviceniicola gen. nov., sp nov and Foliisarcina bertiogensis gen. nov., sp. nov., epiphyllic cyanobacteria associated with Avicennia schaueriana leaves. Int. J. Syst. Evol. Microbiol. 66 689–700. 10.1099/ijsem.0.000774 PubMed DOI

Armbruster U., Labs M., Pribil M., Viola S., Xu W., Scharfenberg M., et al. (2013). Arabidopsis CURVATURE THYLAKOID1 proteins modify thylakoid architecture by inducing membrane curvature. Plant Cell 25 2661–2678. 10.1105/tpc.113.113118 PubMed DOI PMC

Barthel S., Bernát G., Seidel T., Rupprecht E., Kahmann U., Schneider D. (2013). Thylakoid membrane maturation and PSII activation are linked in greening Synechocystis sp PCC 6803 cells. Plant Physiol. 163 1037–1046. 10.1104/pp.113.224428 PubMed DOI PMC

Bohunická M., Mareš J., Hrouzek P., Urajová P., Lukeš M., Šmarda J., et al. (2015a). A combined morphological, ultrastructural, molecular, and biochemical study of the peculiar family Gomontiellaceae (oscillatoriales) reveals a new cylindrospermopsin-producing clade of cyanobacteria. J. Phycol. 51 1040–1054. 10.1111/jpy.12354 PubMed DOI

Bohunická M., Pietrasiak N., Johansen J. R., Berrendero-Gómez E., Hauer T., Gaysina L. A., et al. (2015b). Roholtiella, gen. nov (Nostocales, Cyanobacteria)-a tapering and branching cyanobacteria of the family Nostocaceae. Phytotaxa 197 84–103. 10.11646/phytotaxa.197.2.2 DOI

Boudiére L., Michaud M., Petroutsos D., Rebeille F., Falconet D., Bastien O., et al. (2014). Glycerolipids in photosynthesis: composition, synthesis and trafficking. Biochim. Biophys. Acta 1837 470–480. 10.1016/j.bbabio.2013.09.007 PubMed DOI

Brito A., Ramos V., Seabra R., Santos A., Santos C. L., Lopo M., et al. (2012). Culture-dependent characterization of cyanobacterial diversity in the intertidal zones of the Portuguese coast: a polyphasic study. Syst. Appl. Microbiol. 35 110–119. 10.1016/j.syapm.2011.07.003 PubMed DOI

Bruno L., Billi D., Bellezza S., Albertano P. (2009). Cytomorphological and genetic characterization of troglobitic Leptolyngbya strains isolated from Roman hypogea. Appl. Environ. Microbiol. 75 608–617. 10.1128/AEM.01183-08 PubMed DOI PMC

Bryan S. J., Burroughs N. J., Evered C., Sacharz J., Nenninger A., Mullineaux C. W., et al. (2011). Loss of the SPHF homologue Slr1768 leads to a catastrophic failure in the maintenance of thylakoid membranes in Synechocystis sp. PCC 6803. PLoS One 6:e19625. 10.1371/journal.pone.0019625 PubMed DOI PMC

Camacho C., Coulouris G., Avagyan V., Ma N., Papadopoulos J., Bealer K., et al. (2009). BLAST plus: architecture and applications. BMC Bioinformatics 10:421. 10.1186/1471-2105-10-421 PubMed DOI PMC

Casamatta D., Stanic D., Gantar M., Richardson L. L. (2012). Characterization of Roseofilum reptotaenium (Oscillatoriales, Cyanobacteria) gen. et sp. nov. isolated from Caribbean black band disease. Phycologia 51 489–499. 10.2216/11-10.1 DOI

Castenholz R. (2001). “General characteristics of cyanobacteria,” in Bergey’s Manual of Systematic Bacteriology ed. Garrity G. M. (New York, NY: Springer; ), 474–478.

Castenholz R. W., Norris T. B. (2005). Revisionary concepts of species in the Cyanobacteria and their applications. Arch. Hydrobiol. Suppl. 159 53–69. 10.1127/1864-1318/2005/0117-0053 DOI

Cellamare M., Duval C., Drelin Y., Djediat C., Touibi N., Agogue H., et al. (2018). Characterization of phototrophic microorganisms and description of new cyanobacteria isolated from the saline-alkaline crater-lake Dziani Dzaha (Mayotte, Indian Ocean). FEMS Microbiol. Ecol. 94:fiy108. 10.1093/femsec/fiy108 PubMed DOI

Chatchawan T., Komárek J., Strunecký O., Šmarda J., Peerapornpisal Y. (2012). Oxynema, a new genus separated from the genus Phormidium (Cyanophyta). Cryptogam. Algol. 33 41–59. 10.7872/crya.v33.iss1.2011.041 PubMed DOI

Chigri F., Fuchs M., Otters S., Vothknecht U. C. (2012). Thylakoid membrane formation: Vipp1 and more. J. Endocyt.Cell Res. 23 6–10.

Choi D. H., Noh J. H., Lee C. M., Rho S. (2008). Rubidibacter lacunae gen. nov., sp. nov., a unicellular, phycoerythrin-containing cyanobacterium isolated from seawater of Chuuk lagoon, Micronesia. Int. J. Syst. Evol. Microbiol. 58 2807–2811. 10.1099/ijs.0.65798-0 PubMed DOI

Cohen-Bazire G. S. (1988). Fine-structure of cyanobacteria. Methods Enzymol. 167 157–172. 10.1016/0076-6879(88)67017-0 DOI

Dadheech P. K., Mahmoud H., Kotut K., Krienitz L. (2014). Desertifilum fontinale sp. Nov. (Oscillatoriales, Cyanobacteria) from a warm spring in East Africa, based on conventional and molecular studies. Fottea 14 129–140. 10.5507/fot.2014.010 DOI

Darriba D., Taboada G. L., Doallo R., Posada D. (2012). jModelTest 2: more models, new heuristics and parallel computing. Nat. Methods 9:772. 10.1038/nmeth.2109 PubMed DOI PMC

Dell Inc. (2016). Dell Statistica (Data Analysis Software System), version 13. Available at: software.dell.com

Demé B., Cataye C., Block M. A., Marechal E., Jouhet J. (2014). Contribution of galactoglycerolipids to the 3-dimensional architecture of thylakoids. FASEB J. 28 3373–3383. 10.1096/fj.13-247395 PubMed DOI

Dvořák P., Casamatta D. A., Poulíčková A., Hašler P., Ondřej V., Sanges R. (2014). Synechococcus: 3 billion years of global dominance. Mol. Ecol. 23 5538–5551. 10.1111/mec.12948 PubMed DOI

Dvořák P., Poulíčková A., Hašler P., Belli M., Casamatta D. A., Papini A. (2015). Species concepts and speciation factors in cyanobacteria, with connection to the problems of diversity and classification. Biodivers. Conserv. 24 739–757. 10.1007/s10531-015-0888-6 DOI

Engene N., Rottacker E. C., Kaštovský J., Byrum T., Choi H., Ellisman M. H., et al. (2012). Moorea producens gen. nov., sp. nov. and Moorea bouillonii comb. nov., tropical marine cyanobacteria rich in bioactive secondary metabolites. Int. J. Syst. Evol. Microbiol. 62 1171–1178. 10.1099/ijs.0.033761-0 PubMed DOI PMC

Fiore M. F., Sant’Anna C. L., Azevedo M. T. D., Komárek J., Kaštovský J., Sulek J., et al. (2007). The cyanobacterial genus Brasilonema, gen. nov., a molecular and phenotypic evaluation. J. Phycol. 43 789–798. 10.1111/j.1529-8817.2007.00376.x PubMed DOI

Flombaum P., Gallegos L. L., Gordillo R. A., Rincon J., Zabala L. L., Jiao N., et al. (2013). Present and future global distributions of the marine Cyanobacteria Prochlorococcus and Synechococcus. Proc. Natl. Acad. Sci. U.S.A. 110 9824–9829. 10.1073/pnas.1307701110 PubMed DOI PMC

Flores E., Herrero A. (2010). Compartmentalized function through cell differentiation in filamentous cyanobacteria. Nat. Rev. Microbiol. 8 39–50. 10.1038/nrmicro2242 PubMed DOI

Gantt E., Conti S. F. (1969). Ultrastructure of blue-green algae. J. Bacteriol. 97 1486–1493. PubMed PMC

Gonzalez-Esquer C. R., Šmarda J., Rippka R., Axen S. D., Guglielmi G., Gugger M., et al. (2016). Cyanobacterial ultrastructure in light of genomic sequence data. Photosynth. Res. 129 147–157. 10.1007/s11120-016-0286-2 PubMed DOI

Gugger M. F., Hoffmann L. (2004). Polyphyly of true branching cyanobacteria (Stigonematales). Int. J. Syst. Evol. Microbiol. 54 349–357. 10.1099/ijs.0.02744-0 PubMed DOI

Guglielmi G., Cohen-Bazire G. (1984). Etude taxonomique d’un genre de cyanobacterie Oscillatoriacee: le genre Pseudanabaena Lauterborn. II. Analyse de la composition moleculaire et de la structure des phycobilisomes. Protistologica 20 393–493.

Guglielmi G., Cohen-Bazire G., Bryant D. A. (1981). The structure of Gloeobacter violaceus and its phycobilisomes. Arch. Microbiol. 129 181–189. 10.1007/bf00425248 DOI

Harris L. K., Theriot J. A. (2016). Relative rates of surface and volume synthesis set bacterial cell size. Cell 165 1479–1492. 10.1016/j.cell.2016.05.045 PubMed DOI PMC

Hašler P., Casamatta D., Dvořák P., Poulíčková A. (2017). Jacksonvillea apiculata (Oscillatoriales, Cyanobacteria) gen. & sp. nov.: a new genus of filamentous, epipsamic cyanobacteria from North Florida. Phycologia 56 284–295. 10.2216/16.62.1 DOI

Heinz S., Rast A., Shao L., Gutu A., Guegel I. L., Heyno E., et al. (2016). Thylakoid membrane architecture in Synechocystis depends on CurT, a homolog of the granal CURVATURE THYLAKOID1 Proteins. Plant Cell 28 2238–2260. 10.1105/tpc.16.00491 PubMed DOI PMC

Herbstová M., Tietz S., Kinzel C., Turkina M. V., Kirchhoff H. (2012). Architectural switch in plant photosynthetic membranes induced by light stress. Proc. Natl. Acad. Sci. U.S.A. 109 20130–20135. 10.1073/pnas.1214265109 PubMed DOI PMC

Hoffmann L. (1988). Criteria for the classification of blue-green algae (cyanobacteria) at the genus and at the species levels. Arch. Hydrobiol. 5 131–139.

Hoffmann L., Kaštovský J., Komárek J. (2005). System of cyanoprokaryotes (cyanobacteria) – state in 2004. Algol. Stud. 117 95–115. 10.1127/1864-1318/2005/0117-0095 PubMed DOI

Järvi S., Gollan P. J., Aro E.-M. (2013). Understanding the roles of the thylakoid lumen in photosynthesis regulation. Front. Plant Sci. 4:434. 10.3389/fpls.2013.00434 PubMed DOI PMC

Jehl P., Sievers F., Higgins D. G. (2015). OD-seq: outlier detection in multiple sequence alignments. BMC Bioinformatics 16:269. 10.1186/s12859-015-0702-1 PubMed DOI PMC

Johansen J. R., Casamatta D. A. (2005). Recognizing cyanobacterial diversity through adoption of a new species paradigm. Algol. Stud. 117 71–93. 10.1127/1864-1318/2005/0117-0071 DOI

Kaštovský J., Johansen J. R. (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 47 307–320. 10.2216/07-69.1 DOI

Katoh K., Standley D. M. (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30 772–780. 10.1093/molbev/mst010 PubMed DOI PMC

Keeling P. J. (2013). The number, speed, and impact of plastid endosymbioses in eukaryotic evolution. Ann. Rev. Plant Biol. 64 583–607. 10.1146/annurev-arplant-050312-120144 PubMed DOI

Kirchhoff H. (2013). Architectural switches in plant thylakoid membranes. Photosynth. Res. 116 481–487. 10.1007/s11120-013-9843-0 PubMed DOI

Kirchhoff H., Mukherjee U., Galla H. J. (2002). Molecular architecture of the thylakoid membrane: lipid diffusion space for plastoquinone. Biochemistry 41 4872–4882. 10.1021/bi011650y PubMed DOI

Klotz A., Georg J., Bučinská L., Watanabe S., Reimann V., Januszewski W., et al. (2016). Awakening of a dormant cyanobacterium from nitrogen chlorosis reveals a genetically determined program. Curr. Biol. 26 2862–2872. 10.1016/j.cub.2016.08.054 PubMed DOI

Komárek J. (2018). Several problems of the polyphasic approach in the modern cyanobacterial system. Hydrobiologia 811 7–17. 10.1007/s10750-017-3379-9 DOI

Komárek J., Čáslavská J. (1991). Thylakoidal patterns in oscillatorialean genera. Arch. Hydrobiol. 64 267–270.

Komárek J., Cepák V. (1998). Cytomorphological characters supporting the taxonomic validity of Cyanothece (Cyanoprokaryota). Plant Syst. Evol. 210 25–39. 10.1007/bf00984725 DOI

Komárek J., Cepák V., Kaštovský J., Sulek J. (2004). What are the cyanobacterial genera Cyanothece and Cyanobacterium? Contribution to the combined molecular and phenotype taxonomic evaluation of cyanobacterial diversity. Arch. Hydrobiol. Suppl. 153 1–36. 10.1127/1864-1318/2004/0113-0001 DOI

Komárek J., Kaštovský J. (2003). Coincidences of structural and molecular characters in evolutionary lines of cyanobacteria. Algol. Stud. 148 305–325. 10.1127/1864-1318/2003/0109-0305 DOI

Komárek J., Kaštovský J., Mareš J., Johansen J. R. (2014). Taxonomic classification of cyanoprokaryotes (cyanobacterial genera) 2014, using a polyphasic approach. Preslia 86 295–335.

Komárek J., Kaśtovský J., Ventura S., Turicchia S., Šmarda J. (2009). The cyanobacterial genus Phormidesmis. Algol. Stud. 129 41–59. 10.1127/1864-1318/2009/0129-0041 PubMed DOI

Komárek J., Zapomělová E., Šmarda J., Kopecký J., Rejmánková E., Woodhouse J., et al. (2013). Polyphasic evaluation of Limnoraphis robusta, a water-bloom forming cyanobacterium from Lake Atitlán, Guatemala, with a description of Limnoraphis gen. nov. Fottea 13 39–52. 10.5507/fot.2013.004 DOI

Komenda J., Sobotka R., Nixon P. J. (2012). Assembling and maintaining the photosystem II complex in chloroplasts and cyanobacteria. Curr. Opin. Plant Biol. 15 245–251. 10.1016/j.pbi.2012.01.017 PubMed DOI

Korelusová J., Kaštovský J., Komárek J. (2009). Heterogeneity of the cyanobacterial genus Synechocystis and description of a new genus, Geminocystis. J. Phycol. 45 928–937. 10.1111/j.1529-8817.2009.00701.x PubMed DOI

Kowalewska L., Mazur R., Suski S., Garstka M., Mostowska A. (2016). Three-dimensional visualization of the tubular-lamellar transformation of the internal plastid membrane network during Runner Bean chloroplast biogenesis. Plant Cell 28 875–891. 10.1105/tpc.15.01053 PubMed DOI PMC

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. 10.1093/molbey/msy096 PubMed DOI PMC

Kunkel D. D. (1982). Thylakoid centers - structures associated with the cyanobacterial photosynthetic membrane system. Arch. Microbiol. 133 97–99. 10.1007/bf00413518 DOI

Kwon K. C., Cho M. H. (2008). Deletion of the chloroplast-localized AtTerC gene product in Arabidopsis thaliana leads to loss of the thylakoid membrane and to seedling lethality. Plant J. 55 428–442. 10.1111/j.1365-313X.2008.03523.x PubMed DOI

Lamprinou V., Hernández-Mariné M., Pachiadaki M. G., Kormas K. A., Economou-Amilli A., Pantazidou A. (2013). New findings on the true-branched monotypic genus Iphinoe (Cyanobacteria) from geographically isolated caves (Greece). Fottea 13 15–23. 10.5507/fot.2013.002 DOI

Lamprinou V., Skaraki K., Kotoulas G., Economou-Amilli A., Pantazidou A. (2012). Toxopsis calypsus gen. nov., sp nov (Cyanobacteria, Nostocales) from cave ’Francthi’, Peloponnese, Greece: a morphological and molecular evaluation. Int. J. Syst. Evol. Microbiol. 62 2870–2877. 10.1099/ijs.0.038679-0 PubMed DOI

Lang N. J. (1968). Fine structure of blue-green algae. Annu. Rev. Microbiol. 22 15–46. 10.1146/annurev.mi.22.100168.000311 PubMed DOI

Liberton M., Austin J. R., II, Berg R. H., Pakrasi H. B. (2011a). Insights into the complex 3-D architecture of thylakoid membranes in unicellular cyanobacterium Cyanothece sp. ATCC 51142. Plant Signal. Behav. 6 566–569. PubMed PMC

Liberton M., Austin J. R., II, Berg R. H., Pakrasi H. B. (2011b). Unique thylakoid membrane architecture of a unicellular N2-fixing cyanobacterium revealed by electron tomography. Plant Physiol. 155 1656–1666. 10.1104/pp.110.165332 PubMed DOI PMC

Liberton M., Berg R. H., Heuser J., Roth R., Pakrasi H. B. (2006). Ultrastructure of the membrane systems in the unicellular cyanobacterium Synechocystis sp. strain PCC 6803. Protoplasma 227 129–138. 10.1007/s00709-006-0145-7 PubMed DOI

Lokmer A. (2007). Polyphasic Approach to the Taxonomy of the Selected Oscillatoria Strains (Cyanobacteria). Master’s thesis, University of South Bohemia, České Budějovice, CZ.

Maddison W. P., Maddison D. R. (2018). Mesquite: A Modular System for Evolutionary Analysis, 3.51 edn. Available at: www.mesquiteproject.org

Mareš J. (2018). Multilocus and SSU rRNA gene phylogenetic analyses of available cyanobacterial genomes, and their relation to the current taxonomic system. Hydrobiologia 811 19–34. 10.1007/s10750-017-3373-2 DOI

Mareš J., Hrouzek P., Kaňa R., Ventura S., Strunecký O., Komárek J. (2013). The primitive thylakoid-less cyanobacterium Gloeobacter is a common rock-dwelling organism. PLoS One 8:e66323. 10.1371/journal.pone.0066323 PubMed DOI PMC

Mareš J., Lara Y., Dadáková I., Hauer T., Uher B., Wilmotte A., et al. (2015). Phylogenetic analysis of cultivation-resistant terrestrial cyanobacteria with massive sheaths (Stigonema spp. and Petalonema alatum, Nostocales, Cyanobacteria) using single-cell and filament sequencing of environmental samples. J. Phycol. 51 288–297. 10.1111/jpy.12273 PubMed DOI

Mareš J., Strunecký O., Bučinská L., Wiedermannová J. (2018). Data from: Evolutionary Patterns of Thylakoid Architecture in Cyanobacteria. Figshare. Avialable at: https://figshare.com/articles/supplementary_trees_Mares_etal_rar/7539875 PubMed PMC

Martins M. D., Rigonato J., Taboga S. R., Branco L. H. Z. (2016). Proposal of Ancylothrix gen. nov., a new genus of Phormidiaceae (Cyanobacteria, Oscillatoriales) based on a polyphasic approach. Int. J. Syst. Evol. Microbiol. 66 2396–2405. 10.1099/ijsem.0.001044 PubMed DOI

Miller M. A., Pfeiffer W., Schwartz T. (2012). “The CIPRES science gateway: enabling high-impact science for phylogenetics researchers with limited resources,” in Proceedings of the 1st Conference of the Extreme Science and Engineering Discovery Environment: Bridging from the eXtreme to the Campus and Beyond Chicago, IL: 10.1145/2335755.2335836 DOI

Montgomery B. L. (2015). Light-dependent governance of cell shape dimensions in cyanobacteria. Front. Microbiol. 6:514. 10.3389/fmicb.2015.00514 PubMed DOI PMC

Mühlsteinová R., Johansen J. R., Pietrasiak N., Martin M. P. (2014a). Polyphasic characterization of Kastovskya adunca gen. nov. et comb. nov. (Cyanobacteria: Oscillatoriales), from desert soils of the Atacama Desert, Chile. Phytotaxa 163 216–228. 10.11646/phytotaxa.163.4.2 DOI

Mühlsteinová R., Johansen J. R., Pietrasiak N., Martin M. P., Osorio-Santos K., Warren S. D. (2014b). Polyphasic characterization of Trichocoleus desertorum sp. nov. (Pseudanabaenales, Cyanobacteria) from desert soils and phylogenetic placement of the genus Trichocoleus. Phytotaxa 163 241–261. 10.11646/phytotaxa.163.5.1 DOI

Mullineaux C. W. (2014). Co-existence of photosynthetic and respiratory activities in cyanobacterial thylakoid membranes. Biochim. Biophys. Acta 1837 503–511. 10.1016/j.bbabio.2013.11.017 PubMed DOI

Mustardy L., Garab G. (2003). Granum revisited. A three -dimensional model - where things fall into place. Trends Plant Sci. 8 117–122. 10.1016/s1360-1385(03)00015-3 PubMed DOI

Nguyen L. T. T., Cronberg G., Moestrup O., Daugbjerg N. (2013). Annamia toxica gen. et sp. nov. (Cyanobacteria), a freshwater cyanobacterium from Vietnam that produces microcystins: ultrastructure, toxicity and molecular phylogenetics. Phycologia 52 25–36. 10.2216/10-097.1 DOI

Nickelsen J., Rengstl B., Stengel A., Schottkowski M., Soll J., Ankele E. (2011). Biogenesis of the cyanobacterial thylakoid membrane system - an update. FEMS Microbiol. Lett. 315 1–5. 10.1111/j.1574-6968.2010.02096.x PubMed DOI

Nickelsen J., Zerges W. (2013). Thylakoid biogenesis has joined the new era of bacterial cell biology. Front. Plant Sci. 4:458. 10.3389/fpls.2013.00458 PubMed DOI PMC

Nierzwicki-Bauer S. A., Balkwill D. L., Stevens S. E., Jr. (1983). Three-dimensional ultrastructure of a unicellular cyanobacterium. J. Cell Biol. 97 713–722. 10.1083/jcb.97.3.713 PubMed DOI PMC

Novis P. M., Visnovsky G. (2011). Novel alpine algae from New Zealand: cyanobacteria. Phytotaxa 22 1–24. 10.11646/phytotaxa.22.1.1 DOI

Palinska K. A., Krumbein W. E., Schlemminger U. (1998). Ultramorphological studies on Spirulina sp. Bot. Mar. 41 349–355. 10.1515/botm.1998.41.1-6.349 DOI

Peduzzi P., Gruber M., Schagerl M. (2014). The virus’s tooth: cyanophages affect an African flamingo population in a bottom-up cascade. ISME J. 8 1346–1351. 10.1038/ismej.2013.241 PubMed DOI PMC

Pils B., Copley R. R., Schultz J. (2005). Variation in structural location and amino acid conservation of functional sites in protein domain families. BMC Bioinformatics 6:210. 10.1186/1471-2105-6-210 PubMed DOI PMC

Porta D., Hernández-Mariné M., Herdman M., Rippka R. (2003). Structural and ultrastructural characterization of Symploca atlantica GOMONT, strain PCC 8002 (Oscillatoriales, Cyanophyta, Cyanobacteria). Algol. Stud. 109 509–524. 10.1127/1864-1318/2003/0109-0509 DOI

Pribil M., Labs M., Leister D. (2014). Structure and dynamics of thylakoids in land plants. J. Exp. Bot. 65 1955–1972. 10.1093/jxb/eru090 PubMed DOI

Price M. N., Dehal P. S., Arkin A. P. (2010). Fast tree 2-approximately maximum-likelihood trees for large alignments. PLoS One 5:e9490. 10.1371/journal.pone.0009490 PubMed DOI PMC

Ramirez M., Hernández-Mariné M., Mateo P., Berrendero E., Roldán M. (2011). Polyphasic approach and adaptative strategies of Nostoc cf. commune (Nostocales, Nostocaceae) growing on Mayan monuments. Fottea 11 73–86. 10.5507/fot.2011.008 DOI

Rasoulouniriana D., Siboni N., Ben-Dov E., Kramarsky-Winter E., Loya Y., Kushmaro A. (2009). Pseudoscillatoria coralii gen. nov., sp nov., a cyanobacterium associated with coral black band disease (BBD). Dis. Aquat. Org. 87 91–96. 10.3354/dao02089 PubMed DOI

Rast A., Heinz S., Nickelsen J. (2015). Biogenesis of thylakoid membranes. Biochim. Biophys. Acta 1847 821–830. 10.1016/j.bbabio.2015.01.007 PubMed DOI

Reynolds E. S. (1963). Use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J. Cell Biol. 17 208–212. 10.1083/jcb.17.1.208 PubMed DOI PMC

Ridley C. P., Faulkner D. J., Haygood M. G. (2005). Investigation of Oscillatoria spongeliae-dominated bacterial communities in four dictyoceratid sponges. Appl. Environ. Microbiol. 71 7366–7375. 10.1128/aem.71.11.7366-7375.2005 PubMed DOI PMC

Rigonato J., Gama W. A., Alvarenga D. O., Branco L. H. Z., Brandini F. P., Genuário D. B., et al. (2016). Aliterella atlantica gen. nov., sp. nov., and Aliterella antarctica sp. nov., novel members of coccoid Cyanobacteria. Int. J. Syst. Evol. Microbiol. 66 2853–2861. 10.1099/ijsem.0.001066 PubMed DOI

Rippka R., Cohen-Bazire G. (1983). The cyanobacteriales - a legitimate order based on the type strain Cyanobacterium stanieri. Ann. Microbiol. B 134 21–36. 10.1016/s0769-2609(83)80094-5 PubMed DOI

Rippka R., Deruelles J., Waterbury J. B., Herdman M., Stanier R. Y. (1979). Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J. Gen. Microbiol. 111 1–61. 10.1099/00221287-111-1-1 DOI

Rippka R., Waterbury J., Cohen-Bazire G. (1974). Cyanobacterium which lacks thylakoids. Arch. Microbiol. 100 419–436. 10.1007/bf00446333 DOI

Ris H., Singh R. N. (1961). Electron microscope studies on blue-green algae. J. Biophys. Biochem. Cytol. 9 63–80. 10.1083/jcb.9.1.63 PubMed DOI PMC

Ronquist F., Teslenko M., van der Mark P., Ayres D. L., Darling A., Hohna S., et al. (2012). MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61 539–542. 10.1093/sysbio/sys029 PubMed DOI PMC

Schirrmeister B. E., Antonelli A., Bagheri B. C. (2011). The origin of multicellularity in cyanobacteria. BMC Evol. Biol. 11:45. 10.1186/1471-2148-11-45 PubMed DOI PMC

Schirrmeister B. E., Gugger M., Donoghue P. C. J. (2015). Cyanobacteria and the great oxidation event: evidence from genes and fossils. Palaeontology 58 769–785. 10.1111/pala.12178 PubMed DOI PMC

Schirrmeister B. E., Sanchez-Baracaldo P., Wacey D. (2016). Cyanobacterial evolution during the Precambrian. Int. J. Astrobiol. 15 187–204. 10.1017/s1473550415000579 DOI

Sela I., Ashkenazy H., Katoh K., Pupko T. (2015). GUIDANCE2: accurate detection of unreliable alignment regions accounting for the uncertainty of multiple parameters. Nucleic Acids Res. 43 W7–W14. 10.1093/nar/gkv318 PubMed DOI PMC

Shalygin S., Shalygina R., Johansen J. R., Pietrasiak N., Berrendero-Gómez E., Bohunická M., et al. (2017). Cyanomargarita gen. nov. (Nostocales, Cyanobacteria): convergent evolution resulting in a cryptic genus. J. Phycol. 53 762–777. 10.1111/jpy.12542 PubMed DOI

Shimoni E., Rav-Hon O., Ohad I., Brumfeld V., Reich Z. (2005). Three-dimensional organization of higher-plant chloroplast thylakoid membranes revealed by electron tomography. Plant Cell 17 2580–2586. 10.1105/tpc.105.035030 PubMed DOI PMC

Sinetova M. A., Bolatkhan K., Sidorov R. A., Mironov K. S., Skrypnik A. N., Kupriyanova E. V., et al. (2017). Polyphasic characterization of the thermotolerant cyanobacterium Desertifilum sp. strain IPPAS B-1220. FEMS Microbiol. Lett. 364:fnx027. 10.1093/femsle/fnx027 PubMed DOI

Spurr A. R. (1969). A low-viscosity epoxy resin embedding medium for electron microscopy. J. Ultrastruct. Res. 26 31–43. 10.1016/s0022-5320(69)90033-1 PubMed DOI

Standfuss J., Van Scheltinga A. C. T., Lamborghini M., Kuehlbrandt W. (2005). Mechanisms of photoprotection and nonphotochemical quenching in pea light-harvesting complex at 2.5A resolution. EMBO J. 24 919–928. 10.1038/sj.emboj.7600585 PubMed DOI PMC

Strunecký O., Bohunická M., Johansen J. R., Ćapková K., Raabová L., Dvořák P., et al. (2017). A revision of the genus Geitlerinema and a description of the genus Anagnostidinema gen. nov (Oscillatoriophycidae, Cyanobacteria). Fottea 17 114–126. 10.5507/fot.2016.025 DOI

Strunecký O., Elster J., Komárek J. (2011). Taxonomic revision of the freshwater cyanobacterium ”Phormidium” murrayi = Wilmottia murrayi. Fottea 11 57–71. 10.5507/fot.2011.007 DOI

Strunecký O., Komárek J., Johansen J., Lukešová A., Elster J. (2013). Molecular and morphological criteria for revision of the genus Microcoleus (Oscillatoriales, cyanobacteria). J. Phycol. 49 1167–1180. 10.1111/jpy.12128 PubMed DOI

Strunecký O., Komárek J., Šmarda J. (2014). Kamptonema (Microcoleaceae, Cyanobacteria), a new genus derived from the polyphyletic Phormidium on the basis of combined molecular and cytomorphological markers. Preslia 86 193–208.

Sundberg E., Slagter J. G., Fridborg I., Cleary S. P., Robinson C., Coupland G. (1997). ALBINO3, an Arabidopsis nuclear gene essential for chloroplast differentiation, encodes a chloroplast protein that shows homology to proteins present in bacterial membranes and yeast mitochondria. Plant Cell 9 717–730. 10.1105/tpc.9.5.717 PubMed DOI PMC

Taton A., Wilmotte A., Śmarda J., Elster J., Komárek J. (2011). Plectolyngbya hodgsonii: a novel filamentous cyanobacterium from Antarctic lakes. Polar Biol. 34 181–191. 10.1007/s00300-010-0868-y DOI

Theis J., Schroda M. (2016). Revisiting the photosystem II repair cycle. Plant Signal. Behav. 11:e1218587. 10.1080/15592324.2016.1218587 PubMed DOI PMC

Ting C. S., Hsieh C., Sundararaman S., Mannella C., Marko M. (2007). Cryo-electron tomography reveals the comparative three-dimensional architecture of Prochlorococcus, a globally important marine cyanobacterium. J. Bacteriol. 189 4485–4493. 10.1128/jb.01948-06 PubMed DOI PMC

van de Meene A. M. L., Hohmann-Marriott M. F., Vermaas W. F. J., Roberson R. W. (2006). The three-dimensional structure of the cyanobacterium Synechocystis sp. PCC 6803. Arch. Microbiol. 184 259–270. 10.1007/s00203-005-0027-y PubMed DOI

van Eykelenburg C. (1979). The ultrastructure of Spirulina platensis in relation to temperature and light intensity. Antonie Van Leeuwenhoek 45 369–390. 10.1007/BF00443277 PubMed DOI

Whitton B. A. (1972). “Fine structure and taxonomy on the blue-green algae,” in Taxonomy and Biology of Blue-Green Algae ed. Desikachary T. T. (Chennai: University of Madras; ) 18–26.

Wilde S. B., Johansen J. R., Wilde H. D., Jiang P., Bartelme B. A., Haynie R. S. (2014). Aetokthonos hydrillicola gen. et sp. nov.: epiphytic cyanobacteria on invasive aquatic plants implicated in avian vacuolar myelinopathy. Phytotaxa 181 243–260. 10.11646/phytotaxa.181.5.1 DOI

Yokoyama R., Yamamoto H., Kondo M., Takeda S., Ifuku K., Fukao Y., et al. (2016). Grana-localized proteins, RIQ1 and RIQ2, affect the organization of light-harvesting Complex II and grana stacking in Arabidopsis. Plant Cell 28 2261–2275. 10.1105/tpc.16.00296 PubMed DOI PMC

Yoon H. S., Hackett J. D., Ciniglia C., Pinto G., Bhattacharya D. (2004). A molecular timeline for the origin of photosynthetic eukaryotes. Mol. Biol. Evol. 21 809–818. 10.1093/molbev/msh075 PubMed DOI

Zhang S., Shen G., Li Z., Golbeck J. H., Bryant D. A. (2014). Vipp1 is essential for the biogenesis of photosystem I but not thylakoid membranes in Synechococcus sp. PCC 7002. J. Biol. Chem. 289 15904–15914. 10.1074/jbc.M114.555631 PubMed DOI PMC

Zimba P. V., Huang I. S., Foley J. E., Linton E. W. (2017). Identification of a new-to-science cyanobacterium, Toxifilum mysidocida gen. nov. & sp. nov. (cyanobacteria, cyanophyceae). J. Phycol. 53 188–197. 10.1111/jpy.12490 PubMed DOI

Microdomains heterogeneity in the thylakoid membrane proteins visualized by super-resolution microscopy

Protection of nitrogenase from photosynthetic O2 evolution in Trichodesmium: methodological pitfalls and advances over 30 years of research

Evolutionary Patterns of Thylakoid Architecture in Cyanobacteria