Article

Article name CHAMAESIPHON FONTINALIS SP. NOV., A NEW SPECIES OF UNICELLULAR ASYMMETRICALLY DIVIDING CYANOBACTERIA
Authors

Natalia V. Velichko, PhD, Researcher of the Microbiology Department, Faculty of Biology, Saint-Petersburg State University (199034, Russia, Saint-Petersburg, Universitetskaya embankment, 7/9); iD ORCID: https://orcid.org/0000-0002-0540-9425; e-mail: n.velichko@spbu.ru
Anastasia S. Makeeva, Research Engineer of the Microbiology Department, Faculty of Biology, Saint-Petersburg State University (199034, Russia, Saint-Petersburg, Universitetskaya embankment, 7/9); iD ORCID: https://orcid.org/0000-0002-7181-0495; e-mail: anastasimakeeva@mail.ru
Svetlana G. Averina, PhD, Assistant Professor of the Microbiology Department, Faculty of Biology, Saint-Petersburg State University (199034, Russia, Saint-Petersburg, Universitetskaya embankment, 7/9); iD ORCID: https://orcid.org/0000-0003-0890-1834; e-mail: s.averina@spbu.ru
Svetlana V. Smirnova, PhD, Junior Researcher of the Laboratory of Algology, Komarov Botanical Institute RAS (199034, Russia, Saint-Petersburg, Prof. Popova Street, 2); iD ORCID: https://orcid.org/0000-0001-9982-4840; e-mail: ssmirnova@binran.ru

Reference to article

Velichko N.V., Makeeva A.S., Averina S.G., Smirnova S.V. 2023. Chamaesiphon fontinalis sp. nov., a new species of unicellular asymmetrically dividing cyanobacteria. Nature Conservation Research 8(3): 47–60. https://dx.doi.org/10.24189/ncr.2023.023

Section Research articles
DOI https://dx.doi.org/10.24189/ncr.2023.023
Abstract

Extensive brownish biofilms of algal-bacterial communities were found on stones in streams in the Valdaysky National Park (Russia). The dominant unicellular cyanobacteria in biofilms was determined as Chamaesiphon sp. Although species of this genus often occur in the periphyton of fast-flowing waters, many of them have a geographically limited distribution and occur mainly in mountain streams and rivers in Europe. The strain Chamaesiphon sp. CALU 1864 was isolated from epilithic biofilms in the spring Tekunok. We found that it differs from previously described species not only by its unusual purple pigmentation, but also by morphological features. Molecular-genetic analysis of the primary 16S rRNA sequence and secondary structures of the internal transcribed spacer of the ribosomal operon also confirmed its uniqueness. Phylogenetically, the strain represents an independent lineage on the evolutionary tree. Based on the differences found, which provide strong support for its delineation, we propose to consider strain CALU 1864 as a new species, Chamaesiphon fontinalis sp. nov., first discovered in Russia and described in accordance with the current rules of the International Code of Nomenclature for Algae, Fungi and Plants.

Keywords

Chamaesiphonaceae, morphotype, molecular-genetic features, polyphasic taxonomy, Protected Area

Artice information

Received: 22.02.2023. Revised: 26.06.2023. Accepted: 27.06.2023.

The full text of the article
References

Aigner S., Herburger K., Holzinger A., Karsten U. 2018. Epilithic Chamaesiphon (Synechococcales, Cyanobacteria) species in mountain streams of the Alps – interspecific differences in photo-physiological traits. Journal of Applied Phycology 30(2): 1125–1134. DOI: 10.1007/s10811-017-1328-7
Bryant D.A. 1982. Phycoerythrocyanin and phycoerythrin: properties and occurrence in cyanobacteria. Journal of General Microbiology 128(4): 835–844. DOI: 10.1099/00221287-128-4-835
Cantonati M., Komárek J., Montejano G. 2015. Cyanobacteria in ambient springs. Biodiversity and Conservation 24(4): 865–888. DOI: 10.1007/s10531-015-0884-x
Casamatta D.A., Hašler P. 2016. Blue-green algae (Cyanobacteria) in rivers. In: O. Necchi (Ed.): River Algae. Cham: Springer. P. 5–34. DOI: 10.1007/978-3-319-31984-1_2
Castenholz R.W. 2015. General characteristics of the Cyanobacteria. In: Bergey's Manual of Systematic of Archaea and Bacteria. Hobolken, NJ: Wiley. P. 1–23. DOI: 10.1002/9781118960608.cbm00019
Darriba D., Taboada G.L., Doallo R., Posada D. 2012. jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9(8): 772. DOI: 10.1038/nmeth.2109
Doyle J.J., Doyle J.L. 1990. Isolation of plant DNA from fresh tissue. Focus 12: 13–15.
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. Biodiversity and Conservation 24: 739–757. DOI: 10.1007/s10531-015-0888-6
Efimova L.E., Frolova N.L. 2013. Hydrological monitoring within specially protected natural areas. Water: Chemistry and Ecology 5: 20–28. [In Russian]
Gromov B.V., Mamkaeva K.A. 1980. Cell cycle characteristics of Chamaesiphon confervicola, a cyanobacterium forming exospores. Mikrobiologiia 49(4): 551–554.
Guiry M.D., Guiry G.M. 2022. AlgaeBase. Worldwide electronic publication. Galway: National University of Ireland. Available from https://www.algaebase.org
Gutowski A., Foerster J., Doege A., Paul M. 2015. Chamaesiphon species in soft-water streams in Germany: occurrence, ecology and use for bioindication. Algological Studies 148: 33–56. DOI: 10.1127/algol_stud/2015/0220
Herdman M., Castenholz R.W., Waterbury J.B., Rippka R. 2015. Form-Chamaesiphon. In: Bergey's Manual of Systematic of Archaea and Bacteria. Hobolken, NJ: Wiley. P. 1–3. DOI: 10.1002/9781118960608.gbm00410
Hirose Y., Katayama M., Ohtsubo Y., Misawa N., Iioka E., Suda W., Oshima K., Hanaoka M., Tanaka K., Eki T., Ikeuchi M., Kikuchi Y., Ishida M., Hattori M. 2015. Complete genome sequence of cyanobacterium Geminocystis sp. strain NIES-3708, which performs type II complementary chromatic acclimation. Genome Announcements 3(3): e00357-15. DOI: 10.1128/genomeA.00357-15
Hoffmann L., Komárek J., Kaštovský J. 2005. System of cyanoprokaryotes (cyanobacteria) state in 2004. Algological Studies 117: 95–115. DOI: 10.1127/1864-1318/2005/0117-0095
Hollerbach M.M., Kosinskaya E.K., Polyansky V.I. 1953. Key to freshwater algae of the USSR. Vol. 2: Blue-Green Algae. Moscow: Sovetskaya Nauka. 652 p. [In Russian]
Iteman I., Rippka R., Tandeau de Marsac N., Herdman M. 2000. Comparison of conserved structural and regulatory domains within divergent 16S rRNA-23S rRNA spacer sequences of cyanobacteria. Microbiology 146: 1275–1286. DOI: 10.1099/00221287-146-6-1275
Johansen J.R., Casamatta D.A. 2005. Recognizing cyanobacterial diversity through adoption of a new species paradigm. Algological Studies 117: 71–93. DOI: 10.1127/1864-1318/2005/0117-0071
Johansen J.R., Kovacik L., Casamatta D.A., Iková K.F., Kaštovský J. 2011. Utility of 16S-23S ITS sequence and secondary structure for recognition of intrageneric and intergeneric limits within cyanobacterial taxa: Leptolyngbya corticola sp. nov. (Pseudanabaenaceae, Cyanobacteria). Nova Hedwigia 92(3–4): 283–302. DOI: 10.1127/0029-5035/2011/0092-0283
Kim M., Oh H.S., Park S., Chun J. 2014. Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. International Journal of Systematic and Evolutionary Microbiology 64: 346–351. DOI: 10.1099/ijs.0.059774-0
Komárek J. 2016. A polyphasic approach for the taxonomy of cyanobacteria: principles and applications. European Journal of Phycology 51(3): 346–353. DOI: 10.1080/09670262.2016.1163738
Komárek J., Anagnostidis K. 1998. Cyanoprokaryota, 1 Teil: Chroococcales. In: Süsswasserflora von Mitteleuropa. B. 19/1. Jena: Gustav Fischer. 548 p.
Komárek J., Ludvik J. 1982. Cell structure and reproduction process in the Blue-Green alga Chamaesiphon. Plant Systematics and Evolution 139: 267–277. DOI: 10.1007/BF00989329
Komárek J., Kaštovský J., Mareš J., Johansen J.R. 2014. Taxonomic classification of cyanoprokaryotes (cyanobacterial genera) 2014, using a polyphasic approach. Preslia 86(4): 295–335.
Kurmayer R., Christiansen G., Holzinger A., Rott E. 2018. Single colony genetic analysis of epilithic stream algae of the genus Chamaesiphon spp. Hydrobiologia 811(1): 61–75. DOI: 10.1007/s10750-017-3295-z
Lane D.J. 1991. 16S/23S rRNA sequencing. In: Nucleic acid techniques in bacterial systematics. Chichester: John Wiley and Sons. P. 115–175.
Loza V., Berrendero E., Perona E., Mateo P. 2013a. Polyphasic characterization of benthic cyanobacterial diversity from biofilms of the Guadarrama River (Spain): morphological, molecular, and ecological approaches. Journal of Phycology 49(2): 282–297. DOI: 10.1111/jpy.12036
Loza V., Perona E., Mateo P. 2013b. Molecular fingerprinting of cyanobacteria from river biofilms as a water quality monitoring tool. Applied and Environmental Microbiology 79(5): 1459–1472. DOI: 10.1128/AEM.03351-12
Loza V., Morales A., Perona E., Muñoz-Martín M.A., Mateo P. 2018. Fingerprinting Chamaesiphon populations as an approach to assess the quality of running waters. River Research and Applications 34(6): 595–605. DOI: 10.1002/rra.3277
Lowe T.M., Chan P.P. 2016. tRNAscan-SE On-line: integrating search and context for analysis of transfer RNA genes. Nucleic Acids Research 44(W1): 54–57. DOI: 10.1093/nar/gkw413
Mareš J., Cantonati M. 2016. Phylogenetic position of Geitleribactron purpureum (Synechococcales, Cyanobacteria / Cyanophyceae) and its implications for the taxonomy of Chamaesiphonaceae and Leptolyngbyaceae. Fottea 16(1): 104–111. DOI: 10.5507/fot.2016.002
Mareš J., Strunecký O., Bučinská L., Wiedermannová J. 2019. Evolutionary patterns of thylakoid architecture in Cyanobacteria. Frontiers in Microbiology 10: 277. DOI: 10.3389/fmicb.2019.00277
Melekhin A.V., Davydov D.A., Borovichev E.A., Shalygin S.S., Konstantinova N.A. 2019. CRIS – service for input, storage and analysis of the biodiversity data of the cryptogams. Folia Cryptogamica Estonica 56: 99–108. DOI: 10.12697/fce.2019.56.10
Miller M., Pfeiffer W.T., Schwartz T. 2010. Creating the CIPRES science gateway for inference of large phylogenetic trees. Proceedings of the Gateway Computing Environments Workshop 14: 1–8. DOI: 10.1109/GCE.2010.5676129
Morita R.Y. 1975. Psychrophilic bacteria. Bacteriological Reviews 39: 144–167.
Mühlsteinová R., Johansen J.R., Pietrasiak N., Martin M.P., Osorio-Santos K., Warren S.D. 2014. Polyphasic characterization of Trichocoleus desertorum sp. nov. (Pseudanabaenales, Cyanobacteria) from desert soils and phylogenetic placement of the genus Trichocoleus. Phytotaxa 163(5): 241–261. DOI: 10.11646/phylotaxa.163.5.1
Nadeau T.L., Castenholz R.W. 2000. Characterization of psychrophilic oscillatorians (cyanobacteria) from Antarctic meltwater ponds. Journal of Phycology 36(5): 914–923. DOI: 10.1046/j.1529-8817.2000.99201.x
Perona E., Muñoz-Martín M.Á., Berrendero Gómez E. 2022. Chapter 1 – Recent trends of polyphasic approach in taxonomy and cyanobacterial diversity. In: Expanding horizon of cyanobacterial Biology. A volume of developments in microbiology. Elsevier. P. 1–49. DOI: 10.1016/B978-0-323-91202-0.00008-7
Rabenhorst L. 1865. Sectio II. Algas phycochromaceas complectens. In: Flora europaea algarum aquae dulcis et submarinae. Leipzig: Apud Eduardum Kummerum. P. 148–149.
Raina V., Nayak T., Ray L., Kumari K., Suar M. 2019. Chapter 9 – A polyphasic taxonomic approach for designation and description of novel microbial species. In: Microbial Diversity in the Genomic Era. Academic Press. P. 137–152. DOI: 10.1016/B978-0-12-814849-5.00009-5
Ramasamy D., Mishra A.K., Lagier J., Padhmanabhan R., Rossi M., Sentausa E., Raoult D., Fournier P.E. 2014. A polyphasic strategy incorporating genomic data for the taxonomic description of novel bacterial species. International Journal of Systematic and Evolutionary Microbiology 64: 384–391. DOI: 10.1099/ijs.0.057091-0
Reynolds E.S. 1963. Use of lead citrate at high pH as an electron-opaque stain in electron microscopy. Journal of Cell Biology 17(1): 208–212. DOI: 10.1083/jcb.17.1.208
Rippka R., Deruelles J., Waterbury J.B., Herdman M., Stanier R.Y. 1979. Generic assignments, strain histories and properties of pure cultures of cyanobacteria. Journal of General Microbiology 111(1): 1–61. DOI: 10.1099/00221287-111-1-1
Ronquist F., Teslenko M., van der Mark P., Ayres D.L., Darling A.E., Höhna S., Larget B.R., Liu L., Suchard M.A., Huelsenbeck J.P. 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61(3): 539–542. DOI: 10.1093/sysbio/sys029
Rott E. 2008. Chamaesiphon komarekii species nova, a new benthic freshwater chroococcalean species (Cyanophyta/Cyanobacteria) from western coniferous forest streams in British Columbia, Canada. Algological Studies 126: 37–46. DOI: 10.1127/1864-1318/2008/0126-0037
Rott E., Wehr J.D. 2016. The spatio-temporal development of macroalgae in rivers. In: O. Necchi (Ed.): River Algae. Cham: Springer. P. 159–195. DOI: 10.1007/978-3-319-31984-1_8
Sant'Anna C.L., Gama W.A., Azevedo M.T., Komárek J. 2011. New morphospecies of Chamaesiphon (Cyanobacteria) from Atlantic rainforest, Brazil. Fottea 11: 25–30. DOI: 10.5507/FOT.2011.004
Smirnova S.V. 2014. Planktonic Cyanoprokaryota from waterbodies of the National Park «Valdaiskiy». Novosti Systematiki Nizshikh Rastenii 48: 89–103. DOI: 10.31111/nsnr/2014.48.89 [In Russian]
Smirnova S.V. 2015. Benthic Cyanoprokaryota from waterbodies of the National Park «Valdaisky» (Novgorod Region). Novosti Systematiki Nizshikh Rastenii 49: 52–74. DOI: 10.31111/nsnr/2015.49.52 [In Russian]
Smirnova S.V. 2017. Analysis of cyanoprokaryote flora in waterbodies of «Valdaiskiy» National Park (Novgorod Region). Botanicheskii Zhurnal 102(5): 598–617. DOI: 10.1134/S0006813617050027. [In Russian]
Smirnova S.V. 2021. Cyanoprokaryotes from waterbodies of the National Park «Valdaysky» (Novgorod Region). PhD Thesis. Saint Petersburg. 202 p. [In Russian]
Smirnova S.V., Beljakova R.N. 2016. New species of genus Stichosiphon (Cyanoprokaryota) from waterbodies of Valdaysky National Park (Novgorod Region). Botanicheskii Zhurnal 101(12): 1466–1481. DOI: 10.1134/S0006813616120073 [In Russian]
Stanier R.Y., Cohen-Bazire G. 1977. Phototrophic prokaryotes: the Cyanobacteria. Annual Reviews in Microbiology 31: 225–274. DOI: 10.1146/annurev.mi.31.100177.001301
Stanier R.Y., Kunisawa R., Mandel M., Cohen-Bazire G. 1971. Purification and properties of unicellular blue-green algae (order Chroococcales). Bacteriological Reviews 35(2): 171–205. DOI: 10.1128/BR.35.2.171-205.1971
Strunecký O., Ivanova A.P., Mareš J. 2023. An updated classification of cyanobacterial orders and families based on phylogenomic and polyphasic analysis. Journal of Phycology 59(1): 12–51. DOI: 10.1111/jpy.13304
Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28(10): 2731–2739. DOI: 10.1093/molbev/msr121
Tandeau de Marsac N. 1977. Occurrence and nature of chromatic adaptation in cyanobacteria. Journal of Bacteriology 130(1): 82–91. DOI: 10.1128/jb.130.1.82-91.1977
Trifinopoulos J., Nguyen L.T., von Haeseler A., Minh B.Q. 2016. W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Research 44(W1): 232–235. DOI: 10.1093/nar/gkw256
Turland N.J., Wiersma J.H., Barrie F.R., Greuter W., Hawksworth D.L., Herendeen P.S., Knapp S., Kusber W.-H., Li D.-Z., Marhold K., May T.W., McNeill J., Monro A.M., Prado J., Price M.J., Smith G.F. (Eds.). 2018. International Code of Nomenclature for algae, fungi, and plants (Shenzhen Code) adopted by the Nineteenth International Botanical Congress Shenzhen, China, July 2017. In: Regnum Vegetabile. Vol. 159. Glashütten: Koeltz Botanical Books. 254 p. DOI: 10.12705/Code.2018
Vandamme P., Pot B., Gillis M., de Vos P., Kersters K., Swings J. 1996. Polyphasic taxonomy, a consensus approach to bacterial systematics. Microbiology Reviews 60(2): 407–438. DOI: 10.1128/mr.60.2.407-438.1996
Waterbury J.B., Stanier R.Y. 1977. Two unicellular cyanobacteria which reproduce by budding. Archives of Microbiology 115: 249–257. DOI: 10.1007/BF00446449
Wujek D.E., Gretz M.R. 1984. Ultrastructure of the blue-green alga Chamaesiphon incrustans. Cytobios 40(158): 87–93.
Wynn-Williams D.W. 1990. Ecological Aspects of Antarctic Microbiology. In: K.C. Marshall (Ed.): Advances in Microbial Ecology. Vol. 11. Boston: Springer. P. 71–146. DOI: 10.1007/978-1-4684-7612-5_3
Zuker M. 2003. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Research 31(13): 3406–3415. DOI: 10.1093/nar/gkg595