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DOI: http://dx.doi.org/10.11646/phytotaxa.334.2.6

Nodosilinea chupicuarensis sp. nov. (Leptolyngbyaceae, Synechococcales) a subaerial cyanobacterium isolated from a stone monument in central Mexico

JUAN VÁZQUEZ-MARTÍNEZ, JUAN MANUEL GUTIERREZ-VILLAGOMEZ, CITLALI FONSECA-GARCÍA, ENRIQUE RAMÍREZ-CHÁVEZ, MA. LOURDES MONDRAGÓN-SÁNCHEZ, LAILA PARTIDA-MARTÍNEZ, JEFFREY R. JOHANSEN, JORGE MOLINA-TORRES

Abstract


Microorganisms of subaerial biofilms, which develop on the surface of stone monuments, have been widely studied due to their impact on Cultural Heritage deterioration. Nevertheless, these extremophile microorganisms are poorly characterised. In this study, a cyanobacterial strain isolated from an archaeological zone in north-central Mexico was characterised through a polyphasic study based on ecological, morphological, and molecular data. Phylogenetic analyses were done using sequences of the 16S rRNA gene and the 16S-23S ITS region. Based on the polyphasic data, a new species corresponding to the genus Nodosilinea is described. This alkaliphilic species has optimum growth at pH of 9. Its fatty acid profile indicates that C18:1, 9E and C16:0 are its most abundant fatty acids. Extracellular polymeric substance production was verified on this strain. Only a few species of the genus Nodosilinea have been documented and described, and this is the first report of their presence in central Mexico. Hence the name Nodosilinea chupicuarensis sp. nov. is proposed.


Keywords


Leptolyngbyaceae, cyanobacterial exopolysaccharides, Internal Transcribed Spacer (ITS), 16S rRNA gene, subaerial biofilms; Algae

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References


Abed, R.M.M., Garcia-Pichel, F. & Hernández-Mariné, M. (2002) Polyphasic characterization of benthic, moderately halophilic, moderately thermophilic cyanobacteria with very thin trichomes and the proposal of Halomicronema excentricum gen. nov., sp. nov. Archives of Microbiology 177: 361–370.

https://doi.org/10.1007/s00203-001-0390-2

Anagnostidis, K. (2001) Nomenclatural changes in cyanoprokaryotic order Oscillatoriales. Preslia, Praha 73: 359–375.

Anagnostidis, K. & Komárek, J. (1988) Modern approach to the classification system of cyanophytes. 3 - Oscillatoriales. Algological Studies/Archiv für Hydrobiologie Supplement Volumes 50–53: 327–472.

Berrendero Gómez, E., Johansen, J.R., Kastovský, J., Bohuncká, M. & Capková, K. (2016) Macrochaete gen. nov. (Nostocales, Cyanobacteria), a taxon morphologically and molecularly distinct from Calothrix. Journal of Phycology 52: 638–655.

https://doi.org/10.1111/jpy.12425

Bohunická, M., Johansen, J.R. & Fučíková, K. (2011) Tapinothrix clintonii sp. nov. (Pseudanabaenaceae, Cyanobacteria), a new species at the nexus of five genera. Fottea 11: 127–140.

https://doi.org/10.5507/fot.2011.013

Bohunická, M., Pietrasiak, N., Johansen, J.R., Gómez, E.B., Hauer, T., Gaysina, L.A. & Lukešová, A. (2015) Roholtiella , gen. nov. (Nostocales, Cyanobacteria)—a tapering and branching cyanobacteria of the family Nostocaceae. Phytotaxa 197: 84–103.

https://doi.org/10.11646/phytotaxa.197.2.2

Boyer, S.L., Flechtner, V.R. & Johansen, J.R. (2001) Is the 16S-23S rRNA internal transcribed spacer region a good tool for use in molecular systematics and population genetics? A case study in cyanobacteria. Molecular biology and evolution 18: 1057–1069. https://doi.org/10.1093/oxfordjournals.molbev.a003877

Burger-Wiersma, T., Stal, L.J. & Mur, L.R. (1989) Prochlorothrix hollandica gen. nov., sp. nov., a filamentous oxygenic photoautotrophic procaryote containing chlorophylls a and b: assignment to Prochlorotrichaceae fam. nov. and order Prochlorales Florenzano, Balloni, and Materassi 1986, with emendation of the ordinal description. International Journal of Systematic Bacteriology 39(3): 250–257.

https://doi.org/10.1099/00207713-39-3-250

Cary, S.C., McDonald, I.R., Barrett, J.E. & Cowan, D. (2010) On the rocks: the microbiology of Antarctic Dry Valley soils. Nature reviews. Microbiology 8: 129–138.

https://doi.org/10.1038/nrmicro2281

Cutler, N., Oliver, A., Viles, H. & Whiteley, A. (2012) Non-destructive sampling of rock-dwelling microbial communities using sterile adhesive tape. Journal of Microbiological Methods 91: 391–398.

https://doi.org/10.1016/j.mimet.2012.09.022

Dadheech, P. K., Mahmoud, H., Kotut, K. & Krienitz, L. (2012) Haloleptolyngbya alcalis gen. et sp. nov., a new filamentous cyanobacterium from the soda lake Nakuru, Kenya. Hydrobiologia 691: 269–283.

https://doi.org/10.1007/s10750-012-1080-6

Dvorák, P., Hindák, F., Hasler, P., Hindáková, A. & Poulícková, A. (2014) Morphological and molecular studies of Neosynechococcus sphagnicola, gen. et sp. nov. (Cyanobacteria, Synechococcales). Phytotaxa 170: 24–34.

https://doi.org/10.11646/phytotaxa.170.1.3

Eliáš, M., Němcová, Y., Škaloud, P., Neustupa, J., Kaufnerová, V. & Šejnohová, L. (2010) Hylodesmus singaporensis gen. et sp. nov., a new autosporic subaerial green alga (Scenedesmaceae, Chlorophyta) from Singapore. International Journal of Systematic and Evolutionary Microbiology 60: 1224–1235.

https://doi.org/10.1099/ijs.0.012963-0

Erwin, P.M. & Thacker, R.W. (2008) Phototrophic nutrition and symbiont diversity of two Caribbean sponge–cyanobacteria symbioses. Marine Ecology Progress Series 362: 139–147.

https://doi.org/10.3354/meps07464

Fučíková, K., Hall, J.D., Johansen, J.R. & Lowe, R.L. (2008) Desmid flora of the Great Smoky Mountains National Park, USA. Bibliotheca Phycologica 113: 1–59. ISBN 978-3-443-60040-2

Geitler, L. (1932) Cyanophyceae. In: Rabenhorst, L. (Ed.) Kryptogamen-Flora von Deutschland, Österreich und der Schweiz. Ed. 2. Vol. 14. Akademische Verlagsgesellschaft, Leipzig, pp. 1–1136.

Gomont, M. (1892) Monographie des Oscillariées (Nostocacées Homocystées). Annales des Sciences Naturelles, Botanique, Série 7 15: 263–368; 16: 91–264.

Gorbushina, A. A. (2007) Life on the rocks. Environmental microbiology 9: 1613–1631.

https://doi.org/10.1111/j.1462-2920.2007.01301.x

Gorbushina, A.A. & Broughton, W.J. (2009) Microbiology of the atmosphere-rock interface: how biological interactions and physical stresses modulate a sophisticated microbial ecosystem. Annual review of microbiology 63: 431–450.

https://doi.org/10.1146/annurev.micro.091208.073349

Johansen, J.R., Kovacik, L., Casamatta, D.A., Fučiková, K. & 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: 283–302.

https://doi.org/10.1127/0029-5035/2011/0092-0283

Komárek, J. & Anagnostidis, K. (2005) Cyanoprokaryota 2. Teil: Oscillatoriales. In: Budel, B., Gardner, G., Krienitz, L. & Schageri, M. (Eds.) Süßwasserflora von Mitteleuropa, vol. 19/2. Elsevier, Munchen, 759 pp.

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

Kongisser, R.A. (1925) On the methods of studying phytoplankton [in Russian]. Travaux de la Société des Naturalistes de Leningrad 54.

Lane, D.J. (1991) 16S/23S rRNA sequencing. In: Stackebrandt, E. & Goodfellow, M. (Eds.) Nucleic acid techniques in bacterial systematics. John Wiley and Sons, Chichester, United Kingdom, pp. 115–175.

Lang, I., Hodac, L., Friedl, T. & Feussner, I. (2011) Fatty acid profiles and their distribution patterns in microalgae: a comprehensive analysis of more than 2000 strains from the SAG culture collection. BMC Plant Biology 11: 1–16.

https://doi.org/10.1186/1471-2229-11-124

Li, Z. & Brand, J. (2007) Leptolyngbya nodulosa sp. nov. (Oscillatoriaceae), a subtropical marine cyanobacterium that produces a unique multicellular structure. Phycologia 46: 396–401.

https://doi.org/10.2216/06-89.1

Lopes, V.R., Ramos, V., Martins, A., Sousa, M., Welfer, M., Antunes, A & Vasconcelos, V.M. (2012) Phylogenetic, chemical and morphological diversity of cyanobacteria from Portuguese temperate estuaries. Marine Environmental Research 73: 7–16.

https://doi.org/10.1016/j.marenvres.2011.10.005

Lowe, T.M. & Eddy, S.R. (1997) tRNAscan-SE: A program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Research. 25: 955-964.

https://doi.org/10.1093/nar/25.5.0955

Masoudi-Nejad, A., Tonomura, K., Kawashima, S., Moriya, Y., Suzuki, M., Itoh, M., Kanehisa, M., Endo, T. & Goto, S. (2006) EGassembler: online bioinformatics service for large-scale processing, clustering and assembling ESTs and genomic DNA fragments. Nucleic Acids Research. 34: W459–462.

https://doi.org/10.1093/nar/gkl066

Miscoe, L.H., Johansen, J.R., Vaccarino, M.A., Pietrasiak, N. & Sherwood, A.R. (2016) Novel cyanobacteria from caves on Kauai, Hawaii. Bibliotheca Phycologica 120: 75–152. [ISBN 978-3-443-60047-1]

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

https://doi.org/10.11646/phytotaxa.163.4.2

Neustupa, J., Němcová, Y., Veselá, J., Steinová, J. & Škaloud, P. (2013) Leptochlorella corticola gen. et sp. nov. and Kalinella apyrenoidosa sp. nov.: two novel Chlorella-like green microalgae (Trebouxiophyceae, Chlorophyta) from subaerial habitats. International Journal of Systematic and Evolutionary Microbiology 63: 377–387.

https://doi.org/10.1099/ijs.0.047944-0

Noé Porter, M. (1956) Excavations at Chupícuaro, Guanajuato, Mexico. Transactions of the American Philosophical Society 46: 515-637. https://doi.org/10.2307/1005749

Novelo, E., Tavera, R. & Vidal, G. (2011) Las algas en los sitios arqueológicos mayas. Ciencias 104: 26–35.

Ortega-Morales, B.O., Novelo, E., Ramirez, M. & Gaylarde, C.C (2006) Cyanobacterial diversity and ecology on historic monuments in Latin America. Revista Latinoamericana de Microbiología 48 (2): 188–195.

Osorio-Santos, K., Pietrasiak, N., Bohunická, M., Miscoe, L.H., Kováčik, L., Martin, M.P. & Johansen, J.R. (2014) Seven new species of Oculatella (Pseudanabaenales, Cyanobacteria): taxonomically recognizing cryptic diversification. European Journal of Phycology 49: 450–470.

https://doi.org/10.1080/09670262.2014.976843

Perkerson, R.B., Johansen, J.R., Kováčik, L., Brand, J., Kaštovský, J. & Casamatta, D.A. (2011) A unique Pseudanabaenalean (Cyanobacteria) genus Nodosilinea gen. nov. based on morphological and molecular data. Journal of Phycology 47: 1397–1412. https://doi.org/10.1111/j.1529-8817.2011.01077.x

Pietrasiak, N., Mühlsteinova, R., Siegesmund, M.A. & Johansen, J.R. (2014) Phylogenetic placement of Symplocastrum (Phormidiaceae, Cyanophyceae) with a new combination S. californicum and two new species: S. flechtnerae and S. torsivum. Phycologia 53: 529–541.

https://doi.org/10.2216/14-029.1

Ramirez, M., Hernandez-Marine, M., Novelo, E. & Roldan, M. (2010) Cyanobacteria-containing biofilms from a Mayan monument in Palenque, Mexico. Biofouling 26: 399–409.

https://doi.org/10.1080/08927011003660404

Řeháková, K., Johansen, J.R., Casamatta, D.A., 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: 481–502. https://doi.org/10.2216/06-92.1

Řeháková, K., Johansen, J.R., Bowen, M.B., Martin, M.P. & Sheil, C.A. (2014) Variation in secondary structure of the 16S rRNA molecule in cyanobacteria with implications for phylogenetic analysis. Fottea 14: 161–178.

https://doi.org/10.5507/fot.2014.013

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: 1–61.

https://doi.org/10.1099/00221287-111-1-1

Rossi, F. & De Philippis, R. (2015) Role of cyanobacterial exopolysaccharides in phototrophic biofilms and in complex microbial mats. Life 5: 1218–1238.

https://doi.org/10.3390/life5021218

Sahu, A., Pancha, I., Jain, D., Paliwal, C., Ghosh, T., Patidar, S., Bhattacharya, S. & Mishra, S. (2013) Fatty acids as biomarkers of microalgae. Phytochemistry 89: 53–58.

https://doi.org/10.1016/j.phytochem.2013.02.001

Sauvageau, C. (1892) Sur les algues d’eau douce récoltées en Algérie. Bulletin de la Société de Botanique de France 39: 115–117.

Scheerer, S., Ortega-Morales, O. & Gaylarde, C. (2009) Microbial deterioration of stone monuments―An updated overview. Advances in applied microbiology 66: 97–139.

https://doi.org/10.1016/S0065-2164(08)00805-8

Sciuto, K. & Moro, I. (2016) Detection of the new cosmopolitan genus Thermoleptolyngbya (Cyanobacteria, Leptolyngbyaceae) using the 16S rRNA gene and 16S-23S ITS region. Molecular Phylogenetics and Evolution 105: 15–35.

https://doi.org/10.1016/j.ympev.2016.08.010

Sciuto, K., Moschin, E. & Moro, I. (2017) Cryptic cyanobacterial diversity in the Giant Cave (Trieste, Italy): the new genus Timaviella (Leptolyngbyaceae). Cryptogamie, Algologie 38: 1–39.

https://doi.org/10.7872/crya/v38.iss4.2017.285

Siegesmund, M.A., Johansen, J.R., Karsten, U. & Friedl, T. (2008) Coleofasciculus gen. nov. (Cyanobacteria): Morphological and molecular criteria for revision of the genus Microcoleus Gomont. Journal of Phycology 44: 1572–1585.

https://doi.org/10.1111/j.1529-8817.2008.00604.x

Song, G., Jiang, Y. & Li, R. (2015a) Scytolyngbya timoleontis, gen. et sp. nov. (Leptolyngbyaceae, Cyanobacteria): a novel false branching Cyanobacteria from China. Phytotaxa 224: 72–84.

https://doi.org/10.11646/phytotaxa.224.1.5

Song, H., Zhang, Q.I., Liu, G. & Hu, Z. (2015b) Polulichloris henanensis gen. et sp. nov. (Trebouxiophyceae, Chlorophyta), a novel subaerial coccoid green alga. Phytotaxa 218: 137–146.

https://doi.org/10.11646/phytotaxa.218.2.3

Stackebrandt, E. & Ebers, J. (2006) Taxonomic parameters revisited: tarnished gold standards. Microbiology today 33: 152.

Stackebrandt, E. & Goebel, B.M. (1994) Taxonomic note: a place for DNA–DNA reassociation and 16s rRNA sequence analysis in the present species definition in Bacteriology. International Journal of Systematic Bacteriology 44: 846–849.

https://doi.org/10.1099/00207713-44-4-846

Stoyanov, P., Moten, D., Mladenov, R., Dzhambazov, B. & Teneva, I. (2014) Phylogenetic Relationships of Some Filamentous Cyanoprokaryotic Species. Evolutionary Bioinformatics 10: 39–49.

https://doi.org/10.4137/EBO.S13748

Strunecký, O., Bohunická, M., Johansen, J.R., Čapková, K., Raabová, L., Dvořák, P. & Komárek, J. (2017) A revision of the genus Geitlerinema and a description of the genus Anagnostidinema gen. nov. (Oscillatoriophycidae, Cyanobacteria). Fottea 17: 114–126. https://doi.org/10.5507/fot.2016.025

Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. (2013) MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Molecular Biology and Evolution 30:2725-2729.

https://doi.org/10.1093/molbev/mst197

Taton, A., Wilmotte, A., Smarda, J., Elster, J. & Komárek, J. (2011) Plectolyngbya hodgsonii: a novel filamentous cyanobacterium from Antarctic lakes. Polar Biology 34: 181–191.

https://doi.org/10.1007/s00300-010-0868-y

Turicchia, S., Ventura, S., Komárková, J. & Komárek, J. (2009) Taxonomic evaluation of cyanobacterial microflora from alkaline marshes of northern Belize. 2. Diversity of oscillatorialean genera. Nova Hedwigia 89: 165–200.

https://doi.org/10.1127/0029-5035/2009/0089-0165

UNESCO (2016) Mexico—World Heritage List. Available from: http://whc.unesco.org/en/statesparties/mx (accessed 24 June 2016)

Vaccarino, M.A. & Johansen, J.R. (2012) Brasilonema angustatum sp . nov. (Nostocales), a new filamentous cyanobacterial species from the Hawaiian Islands. Journal of Phycology 48: 1178–1186.

https://doi.org/10.1111/j.1529-8817.2012.01203.x

Vasanthakumar, A., DeAraujo, A., Mazurek, J., Schilling, M. & Mitchell, R. (2013) Microbiological survey for analysis of the brown spots on the walls of the tomb of King Tutankhamun. International Biodeterioration & Biodegradation 79: 56–63.

https://doi.org/10.1016/j.ibiod.2013.01.014

Vaz, M.G.M.V., Bonaldo-Genuário, D., Dini-Andreote, A.P., Silva-Malone, C.F., Sant’-Anna, C.L., Barbiero, L. & Fátima-Fiore, M. (2015) Pantanalinema gen. nov. and Alkalinema gen. nov.: two novel pseudanabaenacean genera (Cyanobacteria) isolated from saline-alkaline lakes. International Journal of Systematic and Evolutionary Microbiology 65: 298–308.

https://doi.org/10.1099/ijs.0.070110-0

Vázquez-Martínez, J., Ramírez-Chávez, E., Gutierrez-Villagomez, J.M. & Molina-Torres, J. (2014) Extracellular polysaccharides and biomass production in cyanobacteria isolated from stone monuments in dry zones of Mexico. Journal of Chemical, Biological and Physical Sciences (JCBPS) 4: 33–43.

Vázquez-Nion, D., Rodríguez-Castro, J., López-Rodríguez, M.C., Fernández-Silva, I. & Prieto, B. (2016) Subaerial biofilms on granitic historic buildings: microbial diversity and development of phototrophic multi-species cultures. Biofouling 32: 657–669.

https://doi.org/10.1080/08927014.2016.1183121

Warscheid, T. & Braams, J. (2000) Biodeterioration of stone: a review. International Biodeterioration & Biodegradation 46: 343–368. https://doi.org/10.1016/S0964-8305(00)00109-8

Waterbury, J.B. (2006) The Cyanobacteria—isolation , purification and identification of major groups of Cyanobacteria. In: Dworkin, M., Falkow, S., Rosenberg, E., Schleifer, K.-H. & Stackebrandt, E.H (Eds.) The Prokaryotes. Third. Springer, New York, 1053–1073.

Yarza, P., Yilmaz, P., Pruesse, E., Glöckner, F.O., Ludwig, W., Schleifer, K., Whitman, W.B., Euzéby, J., Amann, R. & Rosselló-Móra, R. (2014) Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences. Nature Reviews Microbiology 12: 635–645.

https://doi.org/10.1038/nrmicro3330

Zammit, G., Billi, D. & Albertano, P. (2012) The subaerophytic cyanobacterium Oculatella subterranea (Oscillatoriales, Cyanophyceae) gen. et sp. nov.: a cytomorphological and molecular description. European Journal of Phycology 47: 341–354.

https://doi.org/10.1080/09670262.2012.717106

Zepeda-García-Moreno, G. (2008) Cañada de la Virgen, Guanajuato. Arqueología Mexicana 16 (92): 48–51.

Zepeda-García-Moreno, G. (2010) Cañada de la Virgen; Refugio de los muertos y los ancestros. México: 1st Ed. Fideicomiso de Administración e Inversión para la Realización de las Actividades de Rescate y Conservación de Sitios Arqueológicos en el estado de Guanajuato, 137 pp.

Zuker, M. (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Research 31: 3406–3415.

https://doi.org/10.1093/nar/gkg595


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