As the taxonomic knowledge of cyanobacteria from terrestrial environments increases, it remains important to analyze biodiversity in areas that have been understudied to fully understand global and endemic diversity. This study was completed as part of a larger algal biodiversity study of the soil biocrusts of San Nicholas Island, California, USA. Among the taxa isolated were several new species in three genera (Atlanticothrix, Pycnacronema, and Konicacronema) which were described from, and previously restricted to, Brazil. New taxa are described herein using a polyphasic approach to cyanobacterial taxonomy that considers morphological, molecular, ecological, and biogeographical factors. Morphological data corroborated by molecular analysis including sequencing of the 16S rRNA gene, and the associated 16S-23S ITS rRNA region was used to delineate three new species of Atlanticothrix, two species of Pycnacronema, and one species of Konicacronema. The overlap of genera from San Nicolas Island and Brazil suggests that cyanobacterial genera may be widely distributed across global hemispheres, whereas the presence of distinct lineages may indicate that this is not true at the species level. Our data suggest that based upon global wind patterns, cyanobacteria in both Northern and Southern hemispheres of the Americas may have a more recent common ancestor in Northern Africa, but this common ancestry is distant enough that speciation has occurred since transatlantic dispersal.

Department of Biology John Carroll University University Heights Ohio USA

Department of Botany Faculty of Science University of South Bohemia České Budějovice Czech Republic

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Alvarenga, D. O., Andreote, A. P. D., Branco, L. H. Z., Delbaje, E., Cruz, R. B., de Mello Varani, A., & Fiore, M. F. (2021). Amazonocrinis nigriterrae gen. nov., sp. nov., Atlanticothrix silvestris gen. nov., sp. nov. and Denronalium phyllosphericum gen. nov., nostocacean cyanobacteria from Brazilian environments. International Journal of Systematic and Evolutionary Microbiology, 71, 1-12. https://doi.org/10.1099/ijsem.0.00481

Baldarelli, L. M., Pietrasiak, N., Osorio-Santos, K., & Johansen, J. R. (2022). Mojavia aguilerae and M. dolomitestris - two new nostocaceae (Cyanobacteria) species from the Americas. Journal of Phycology, 58, 502-516. https://doi.org/10.1111/jpy.13275

Becerra-Absalón, I., Johansen, J. R., Muñoz-Martín, M. A., & Montejano, G. (2018). Chroakolemma gen. nov. (Leptolyngbyaceae, Cyanobacteria) from soil biocrusts in the semi-desert Central Region of Mexico. Phytotaxa, 367, 201-218. https://doi.org/10.11646/phytotaxa.367.3.1

Becerra-Absalón, I., Johansen, J. R., Osorio-Santos, K., & Montejano, G. (2020). Two new Oculatella (Oculatellaceae, Cyanobacteria) species in soil crusts from tropical semi-arid uplands of Mexico. Fottea, 20, 160-170. https://doi.org/10.5507/fot.2020.010

Becking, L. G. M. B. (1934). Geobiologie of inleiding tot de milieukunde (No. 18-19). WP Van Stockum & Zoon.

Belnap, J. (2003). The world at your feet: Desert soil crusts. Frontiers in Ecology and the Environment, 1, 181-189. https://doi.org/10.1890/1540-9295(2003)001[0181:TWAYFD]2.0.CO;2

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(2), 84. https://doi.org/10.11646/phytotaxa.197.2.2

Boyer, S. L., Flechtner, V. R., & Johansen, J. R. (2001). Is the 16S-23S 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

Boyer, S. L., Johansen, J. R., Flechtner, V. R., & Howard, G. L. (2002). Phylogeny and genetic variance in terrestrial Microcoleus (Cyanophyceae) species based on sequence analysis of the 16S rRNA gene and associated 16S-23S ITS region. Journal of Phycology, 38, 1222-1235. https://doi.org/10.1046/j.1529-8817.2002.01168.x

Brown, I., Tringe, S. G., Ivanova, N., Goodwin, L., Shapiro, N., Alcorta, J., Pan, D., Chrisstoserdov, A., Sarkisova, S., & Woyke, T. (2021). High-quality draft genome sequence of the siderophilic and thermophilic Leptolyngbyaceae cyanobacterium JSC-12. Microbiology Resource Announcements, 10, e0049521. https://doi.org/10.1128/mra.00495-21

Büdel, B., Weber, B., Kühl, M., Pfanz, H., Sültemeyer, D., & Wessels, D. (2004). Reshaping of sandstone surfaces by cryptoendolithic cyanobacteria: bioalkalization causes chemical weathering in arid landscapes. Geobiology, 2(4), 261-268. https://doi.org/10.1111/j.1472-4677.2004.00040.x

Carmichael, W. (1986). Isolation, culture, and toxicity testing of toxic freshwater cyanobacteria (blue-green algae). In V. Shilor (Ed.), Fundamental research in homogenous catalysis (Vol. 3, pp. 1249-1262). Gordon & Breach Publ.

Casamatta, D. A., Gomez, S. R., & Johansen, J. R. (2006). Rexia erecta gen. et sp. nov. and Capsosira lowei sp. nov., two newly described cyanobacterial taxa from the Great Smoky Mountain National Park (USA). Hydrobiologia, 561, 13-26. https://doi.org/10.1007/s10750-005-1602-6

Després, V. R., Huffman, J. A., Burrows, S. M., Hoose, C., Safatov, A. S., Buryak, G., Fröhlich-Nowoisky, J., Elbert, W., Andreae, M. O., Pöschl, U., & Jaenicke, R. (2012). Primary biological aerosol particles in the atmosphere: a review. Tellus B: Chemical and Physical Meteorology, 64(1), 15598. https://doi.org/10.3402/tellusb.v64i0.15598

Drummond, A. J., Ho, S. Y. W., Phillips, M. J., & Rambaut, A. (2006). Relaxed phylogenetics and dating with confidence. PLoS Biology, 4, e88. https://doi.org/10.1371/journal.pbio.0040088

Dvořák, P., Hašler, P., & Poulíčková, A. (2012). Phylogeography of the Microcoleus vaginatus (Cyanobacteria) form three continents - a spatial and temporal characterization. PLoS ONE, 7, e40153. https://doi.org/10.1371/journal.pone.0040153

Engelstaedter, S., Tegen, I., & Washington, R. (2006). North African dust emissions and transport. Earth-Science Reviews, 76, 73-100. https://doi.org/10.1016/j.earscirev.2006.06.004

Erwin, P., & Thacker, R. (2008). Cryptic diversity of the symbiotic cyanobacterium Synechococcus spongiarium among sponge hosts. Molecular Ecology, 17, 2937-2947. https://doi.org/10.1111/j.1365-294X.2008.03808.x

Evans, R. D., & Johansen, J. R. (1999). Microbiotic crusts and ecosystem processes. Critical Reviews in Plant Sciences, 18, 183-225. https://doi.org/10.1080/07352689991309199

Flechtner, V. R., Boyer, S. L., Johansen, J. R., & DeNoble, M. L. (2002). Spirirestis rafaelensis gen.et sp. nov. (Cyanophyceae), a new cyanobacterial genus from arid soils. Nova Hedwigia, 74, 1-24. https://doi.org/10.1127/0029-5035/2002/0074-0001

Flechtner, V. R., Johansen, J. R., & Belnap, J. (2008). The biological soil crusts of the San Nicholas Island: Enigmatic algae from a geographically isolated ecosystem. Western North American Naturalist, 68, 405-436. https://doi.org/10.3398/1527-0904-68.4.405

Fox, G. E., Wisotzkey, J. D., & Jurtshuk, P. (1992). How close is close: 16S rRNA sequence identity may not be sufficient to guarantee species identity. International Journal of Systematic Bacteriology, 42(1), 166-170. https://doi.org/10.1099/00207713-42-1-166

Gelman, A., & Rubin, D. B. (1992). Inference from iterative simulation using multiple sequences. Statistical Science, 7, 157-511. https://doi.org/10.1214/ss/1177011136

Gomont, M. (1892). Monographie des Oscillariées (Nostocacées Homocystées). Deuxième partie. - Lyngbyées. Annales des Sciences Naturelles, Botanique, Série 7, 16, 91-264, pls 1-7.

Harper, K. T., & Marble, J. R. (1989). Effect of timing of grazing on soil-surface cryptogamic communities in a Great Basin low-shrub desert: A preliminary report. Great Basin Naturalist, 49, 104-107.

Hentschke, G. S., Johansen, J. R., Pietrasiak, N., Rigonato, J., Firoe, M. F., & Sant'Anna, C. L. (2017). Komarekiella atlantica gen. et sp. nov. (Nostocaceae, Cyanobacteria): A new subaerial taxon from the Atlantic Rainforest and Kauai, Hawaii. Fottea, 17, 178-190.

Jeffries, D. L., Link, S. O., & Klopatek, J. M. (1993). CO2 fluxes of cryptogamic crusts. I. Response to resaturation. New Phytologist, 125, 163-173. https://doi.org/10.1111/j.1469-8137.1993.tb03874.x

Johansen, J. R., Bohunická, M., Lukešová, A., Hrčková, K., Vaccarino, M. A., & Chesarino, N. M. (2014). Morphological and molecular characterization within 26 strains of the genus Cylindrospermum (Nostocaceae, Cyanobacteria), with descriptions of three new species. Journal of Phycology, 50, 187-202. https://doi.org/10.1111/jpy.12150

Johansen, J. R., & Cassamata, D. A. (2005). Recognizing cyanobacterial diversity through the adoption of a new species paradigm. Algological Studies, 117, 71-93. https://doi.org/10.1127/1864-1318/2005/0117-0071

Johansen, J. R., Kovacik, L., Casamatta, D. A., Fučíková, 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

Jung, P., Mikhailyuk, T., Emrich, D., Baumann, K., Dultz, S., & Büdel, B. (2020). Shifting boundaries: Ecological and geographical range expansion based on three new species in the cyanobacterial genera Cyanocohniella, Oculatella, and Aliterella. Journal of Phycology, 56, 1216-1231. https://doi.org/10.1111/jpy.13025

Kaštovský, J., Berrendero Gomez, E., Hladil, J., & Johansen, J. R. (2014). Cyanocohniella calida gen. et sp. nov. (Cyanobacteria: Aphanizomenonaceae) a new cyanobacterium from the thermal springs from Karlovy Vary, Czech Republic. Phytotaxa, 181, 279-292. https://doi.org/10.11646/phytotaxa.181.5.3

Kaštovský, J., Johansen, J. R., Hauerová, R., & Akagha, M. U. (2023). Hot is rich-An enormous diversity of simple trichal cyanobacteria from Yellowstone hot springs. Diversity, 15, 975. https://doi.org/10.3390/d15090975

Kleiner, E. F., & Harper, K. T. (1972). Environment and community organization in the grasslands of Canyonlands National Park. Ecology, 53, 299-309. https://doi.org/10.2307/1934086

Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R., Thompson, J. D., Gibsin, T. J., & Higgins, D. G. (2007). Clustal W and Clustal X version 2.0. Bioinformatics, 23, 2947-2948. https://doi.org/10.1093/bioinformatics/btm404

Luz, R., Cordeiro, R., Kaštovský, J., Johansen, J. R., Dias, E., Fonseca, A., Urbatzka, R., Vasconcelos, V., & Gonçalves, V. (2023). Description of four new filamentous cyanobacterial taxa from freshwater habitats in the Azores Archipelago. Journal of Phycology, 2023, 1-16. https://doi.org/10.1111/jpy.13396

Machado de Lima, N. M., & Branco, L. H. Z. (2020). Biological soil crusts: New genera and species of cyanobacteria from Brazilian semi-arid regions. Phytotaxa, 470, 263-281. https://doi.org/10.11646/PHYTOTAXA.470.4.1

Marshall, W. A., & Chalmers, M. O. (2006). Airborne dispersal of Antarctic terrestrial algae and cyanobacteria. Ecography, 20, 585-594. https://doi.org/10.1111/j.1600-0587.1997.tb00427.x

Martins, M. D., Machado-de-Lima, N. M., & Branco, L. H. Z. (2018). Polyphasic approach using multilocus analyses supports the establishment of the new aerophytic cyanobacterial genus Pycnacronema (Coleofacisculaceae, Oscillatoriales). Journal of Phycology, 55, 146-159. https://doi.org/10.1111/jpy.12805

Mesfin, M., Johansen, J. R., PietrasiakI, N., & Baldarelli, L. M. (2020). Nostoc oromo sp. nov. (Nostocales, Cyanophyceae) from Ethiopia: a new species based on morphological and molecular evidence. Phytotaxa, 433(2), 81-93. https://doi.org/10.11646/phytotaxa.433.2.1

Miller, M. A., Pfeiffer, W., & Schwartz, T. (2010). Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In 2010 gateway computing environments workshop (GCE) (pp. 1-8).

Moreira-Fernandes, V., Giraldo-Silva, A., Roush, D., & Garcia-Pichel, F. (2021). Coleofasciculaceae, a monophyletic home for the Microcoleus steenstrupii complex and other desiccation-tolerant filamentous cyanobacteria. Journal of Phycology, 57, 1563-1579. https://doi.org/10.1111/jpy.13199

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, 241-261. https://doi.org/10.11646/phytotaxa.163.5.1

Nübel, U., Garcia-Pichel, F., & Muyzer, G. (1997). PCR primers to amplify 16S rRNA genes from cyanobacteria. Applied and Environmental Microbiology, 63, 3327-3332. https://doi.org/10.1128/aem.63.8.3327-3332.1997

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

Pietrasiak, N., Mühlsteinová, R., Siegesmund, M., & Johansen, J. R. (2014). Phylogenetic placement of Symplocastrum (Phormidiaceae, Cyanobacteria) with description of two new species: S. flechtnerae and S. torsivum. Phycologia, 53, 529-541. https://doi.org/10.2216/14-029.1

Pietrasiak, N., Osorio-Santos, K., Shalygin, S., Martin, M. P., & Johansen, J. R. (2019). When is a lineage a species? A case study in Myxacorys gen. nov. (Synechococcales: Cyanobacteria) with the description of two new species from the Americas. Journal of Phycology, 55, 976-996. https://doi.org/10.1111/jpy.12897

Pietrasiak, N., Reeve, S., Osorio-Santos, K., Lipson, D. A., & Johansen, J. R. (2021). Trichotorquatus gen. nov. - A new genus of soil cyanobacteria from American drylands. Journal of Phycology, 57, 886-902. https://doi.org/10.1111/jpy.13147

Prospero, J. M., Delany, A. C., Delany, A. C., & Carlson, T. N. (2021). The discovery of African dust transport to the Western Hemisphere and the Saharan air layer: A history. Bulletin of the American Meteorological Society, 102(6), e1239-e1260. https://doi.org/10.1175/BAMS-D-19-0309.1

Rambaut, A. (2009). FigTree, (version) 1.4.3. http://tree.bio.ed.ac.uk/software/figtree.

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, 45, 481-502. https://doi.org/10.2216/06-92.1

Řeháková, K., Mareš, J., Lukešová, A., Zapomělová, E., Bernardová, K., & Hrouzek, P. (2014). Nodularia (Cyanobacteria, Nostocaceae): A phylogenetically uniform genus with variable phenotypes. Phytotaxa, 172, 235-246. https://doi.org/10.11646/phytotaxa.172.3.4

Ronquist, F., Teslenko, M., Van Der Mark, P., Ayres, D. L., Darling, A., Hohna, S., Larget, B., 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, 539-542. https://doi.org/10.1093/sysbio/sys029

Shalygin, S., Shalygina, R. R., Redkina, V. V., Gargas, C. B., & Johansen, J. R. (2020). Description of Stenomitos kolaenensis and S. hiloensis sp. nov. (Leptolyngbyaceae, Cyanobacteria) with an emendation of the genus. Phytotaxa, 440(2), 108-128. https://doi.org/10.11646/phytotaxa.440.2.3

Sherwood, A. R., Carlile, A. L., Vaccarino, M. A., & Johansen, J. R. (2015). Characterization of Hawaiian freshwater and terrestrial cyanobacteria reveals high diversity and numerous putative endemics. Phycological Research, 63, 85-92. https://doi.org/10.1111/pre.12080

Stamatakis, A. (2014). RAxML version 8, a tool for phylogenetic analysis and post- analysis of large phylogenies. Bioinformatics, 30, 1312-1313. https://doi.org/10.1093/bioinformatics/btu033

Strunecký, O., & Ivanova, A. P. (2023). An updated classification of cyanobacterial orders and families based on phylogenomic and polyphasic analysis. Journal of Phycology, 59, 12-51. https://doi.org/10.1111/jpy.13304

Swofford, D. L. (1998). PAUP*. Phylogenetic analysis using parsimony (*and other methods). Version 4.02b. Sinauer Associates.

Weber, B., Belnap, J., Büdel, B., Antoninka, A. J., Barger, N. N., Chaudhary, V. B., Darrouzet-Nardi, A., Eldridge, D. J., Faist, A. M., Ferrenberg, S., Havrilla, C. A., Huber-Sannwald, E., Issa, O. M., Maestre, F. T., Reed, S. C., Rodriguez-Caballero, E., Tucker, C., Young, K. E., Zhang, Y., … Bowker, M. A. (2022). What is a biocrust? A refined, contemporary definition for a broadening research community. Biological Reviews, 97, 1768-1785. https://doi.org/10.1111/brv.12862

West, N. E. (1990). Structure and function of microphytic soil crusts in wildland ecosystems of arid to semiarid regions. Advances in Ecological Research, 20, 179-223. https://doi.org/10.1016/S0065-2504(08)60055-0

West, W., & West, G. S. (1897). Welwitsch's African freshwater algae. Journal of Botany, British and Foreign, 35, 1-7, 33-42, 77-89, 113-122, 172-183, 235-243, 264-272, 297-304, pls 365-369.

Wilmotte, A., Auwera, G. V. D., & Watcher, R. D. (1993). Structure of the 16S rRNA of the thermophilic cyanobacterium Chlorogloeopsis HTF (‘Mastigocladus laminosus hTF’) strain PCC7518, and phylogenetic analysis. FEBS Letters, 317, 96-100. https://doi.org/10.1016/0014-5793(93)81499-P

Zuker, M. (2003). Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Research, 31(13), 3406-3415. https://doi.org/10.1093/nar/gkg595

Molecular characterization of the type species of Kyrtuthrix (Rivulariaceae, Cyanobacteriota) with comparison to Nunduva: Morphologically different but molecularly cryptic genera

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