Cyanobacterial taxonomy is entering the genomic era, but only a few taxonomic studies have employed population genomics, which provides a framework and a multitude of tools to understand species boundaries. Phylogenomic and population genomic analyses previously suggested that several cryptic lineages emerged within the genus Laspinema. Here, we apply population genomics to define boundaries between these lineages and propose two new cryptic species, Laspinema olomoucense and L. palackyanum. Moreover, we sampled soil and puddles across Central Europe and sequenced the 16S rRNA gene and 16S-23S ITS region of the isolated Laspinema strains. Together with database mining of 16S rRNA gene sequences, we determined that the genus Laspinema has a cosmopolitan distribution and inhabits a wide variety of habitats, including freshwater, saline water, mangroves, soil crusts, soils, puddles, and the human body.

Department of Botany Faculty of Science Palacký University Olomouc Olomouc Czech Republic

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Arnold, B. J., Huang, I. T., & Hanage, W. P. (2021). Horizontal gene transfer and adaptive evolution in bacteria. Nature Reviews Microbiology, 20(4), 206–218. https://doi.org/10.1038/s41579‐021‐00650‐4

Bobay, L.‐M., & Ochman, H. (2017). Biological species are universal across Life's domains. Genome Biology and Evolution, 9(3), 491–501. https://doi.org/10.1093/gbe/evx026

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(6), 1057–1069.

Capella‐Gutiérrez, S., Silla‐Martínez, J. M., & Gabaldón, T. (2009). trimAl: A tool for automated alignment trimming in large‐scale phylogenetic analyses. Bioinformatics, 25(15), 1972–1973. https://doi.org/10.1093/BIOINFORMATICS/BTP348

Dadheech, P. K., Casamatta, D. A., Casper, P., & Krienitz, L. (2013). Phormidium etoshii sp. nov. (Oscillatoriales, Cyanobacteria) described from the Etosha pan, Namibia, based on morphological, molecular and ecological features. Fottea, 13(2), 235–244. https://doi.org/10.5507/fot.2013.019

Dvořák, P., Casamatta, D. A., Hašler, P., Jahodářová, E., Norwich, A. R., & Poulíčková, A. (2017). Diversity of the cyanobacteria. In P. Hallenbeck (Ed.), Modern topics in the phototrophic prokaryotes: Environmental and applied aspects (pp. 3–46). Springer. https://doi.org/10.1007/978‐3‐319‐46261‐5_1

Dvořák, P., Casamatta, D. A., Poulíčková, A., Hašler, P., Ondřej, V., & Sanges, R. (2014). Synechococcus: 3 billion years of global dominance. Molecular Ecology, 23(22), 5538–5551. https://doi.org/10.1111/mec.12948

Dvořák, P., Hašler, P., Casamatta, D. A., & Poulíčková, A. (2021). Underestimated cyanobacterial diversity: Trends and perspectives of research in tropical environments. Fottea, 21(2), 110–127. https://doi.org/10.5507/FOT.2021.009

Dvořák, P., Hašler, P., Pitelková, P., Tabáková, P., Casamatta, D. A., & Poulíčková, A. (2017). A new cyanobacterium from the everglades, Florida—Chamaethrix gen. nov. Fottea, 17(2), 269–276. https://doi.org/10.5507/fot.2017.017

Dvořák, P., Hindák, F., Hašler, P., Hindáková, A., & Poulíčková, A. (2014). Morphological and molecular studies of Neosynechococcus sphagnicola, gen. et sp. nov. (Cyanobacteria, Synechococcales). Phytotaxa, 170(1), 24–34. https://doi.org/10.11646/phytotaxa.170.1.3

Dvořák, P., Jahodářová, E., Stanojković, A., Skoupý, S., & Casamatta, D. A. (2023). Population genomics meets the taxonomy of cyanobacteria. Algal Research, 72, 103128. https://doi.org/10.1016/J.ALGAL.2023.103128

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(4), 739–757. https://doi.org/10.1007/s10531‐015‐0888‐6

Edgar, R. C. (2004). MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32(5), 1792–1797. https://doi.org/10.1093/nar/gkh340

Emms, D. M., & Kelly, S. (2015). OrthoFinder: Solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biology, 16(1), 157. https://doi.org/10.1186/s13059‐015‐0721‐2

Engene, N., Rottacker, E. C., Kaštovský, J., Byrum, T., Choi, H., Ellisman, M. H., Komárek, J., & Gerwick, W. H. (2012). Moorea producens gen. nov., sp. nov. and Moorea bouillonii comb. nov., tropical marine cyanobacteria rich in bioactive secondary metabolites. International Journal of Systematic and Evolutionary Microbiology, 62(5), 1171–1178. https://doi.org/10.1099/ijs.0.033761‐0

Flombaum, P., Gallegos, J. L., Gordillo, R. A., Rincón, J., Zabala, L. L., Jiao, N., Karl, D. M., Li, W. K. W., Lomas, M. W., Veneziano, D., Vera, C. S., Vrugt, J. A., & Martiny, A. C. (2013). Present and future global distributions of the marine cyanobacteria Prochlorococcus and Synechococcus. Proceedings of the National Academy of Sciences of the United States of America, 110(24), 9824–9829. https://doi.org/10.1073/pnas.1307701110

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

Hassler, H. B., Probert, B., Moore, C., Lawson, E., Jackson, R. W., Russell, B. T., & Richards, V. P. (2022). Phylogenies of the 16S rRNA gene and its hypervariable regions lack concordance with core genome phylogenies. Microbiome, 10(1), 104. https://doi.org/10.1186/S40168‐022‐01295‐Y

Heidari, F., Zima, J., Riahi, H., & Hauer, T. (2018). New simple trichal cyanobacterial taxa isolated from radioactive thermal springs. Fottea, 18(2), 137–149. https://doi.org/10.5507/FOT.2017.024

Hoang, D. T., Chernomor, O., Von Haeseler, A., Minh, B. Q., & Vinh, L. S. (2018). UFBoot2: Improving the ultrafast bootstrap approximation. Molecular Biology and Evolution, 35(2), 518–522. https://doi.org/10.1093/MOLBEV/MSX281

Jahodářová, E., Dvořák, P., Hašler, P., Holušová, K., & Poulíčková, A. (2018). Elainella gen. Nov.: A new tropical cyanobacterium characterized using a complex genomic approach. European Journal of Phycology, 53(1), 39–51. https://doi.org/10.1080/09670262.2017.1362591

Jain, C., Rodriguez‐R, L. M., Phillippy, A. M., Konstantinidis, K. T., & Aluru, S. (2018). High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries. Nature Communications, 9(1), 1–8. https://doi.org/10.1038/s41467‐018‐07641‐9

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

Johansen, J. R., Mareš, J., Pietrasiak, N., Bohunická, M., Zima, J., Štenclová, L., & Hauer, T. (2017). Highly divergent 16S rRNA sequences in ribosomal operons of Scytonema hyalinum (cyanobacteria). PLoS One, 12(10), e0186393. https://doi.org/10.1371/JOURNAL.PONE.0186393

Kalyaanamoorthy, S., Minh, B. Q., Wong, T. K. F., Von Haeseler, A., & Jermiin, L. S. (2017). ModelFinder: Fast model selection for accurate phylogenetic estimates. Nature Methods, 14(6), 587–589. https://doi.org/10.1038/nmeth.4285

Kim, D., Park, S., & Chun, J. (2021). Introducing EzAAI: A pipeline for high throughput calculations of prokaryotic average amino acid identity. Journal of Microbiology, 59(5), 476–480. https://doi.org/10.1007/S12275‐021‐1154‐0/METRICS

Kollár, J., Poulíčková, A., & Dvořák, P. (2022). On the relativity of species, or the probabilistic solution to the species problem. Molecular Ecology, 31(2), 411–418. https://doi.org/10.1111/MEC.16218

Komárek, J., Johansen, J. R., Šmarda, J., & Strunecký, O. (2020). Phylogeny and taxonomy of Synechococcus‐like cyanobacteria. Fottea, 20(2), 171–191. https://doi.org/10.5507/fot.2020.006

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.

Kumar, S., Stecher, G., Li, M., Knyaz, C., & Tamura, K. (2018). MEGA X: Molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution, 35(6), 1547–1549. https://doi.org/10.1093/MOLBEV/MSY096

Labrada, N. A., McGovern, C. A., Thomas, A. L., Hurley, A. C., Mooney, M. R., & Casamatta, D. A. (2023). The CIMS (cyanobacterial ITS motif slicer) for molecular systematics. Fottea, 24, 23–26. https://doi.org/10.5507/FOT.2023.008

Larsson, A. (2014). AliView: A fast and lightweight alignment viewer and editor for large datasets. Bioinformatics, 30(22), 3276–3278. https://doi.org/10.1093/BIOINFORMATICS/BTU531

Mayr, E. (1942). Systematics and the origin of species. Columbia University Press.

Nabout, J. C., da Silva Rocha, B., Carneiro, F. M., & Sant'Anna, C. L. (2013). How many species of cyanobacteria are there? Using a discovery curve to predict the species number. Biodiversity and Conservation, 22(12), 2907–2918. https://doi.org/10.1007/s10531‐013‐0561‐x

Nguyen, L.‐T., Schmidt, H. A., von Haeseler, A., & Minh, B. Q. (2015). IQ‐TREE: A fast and effective stochastic algorithm for estimating maximum‐likelihood phylogenies. Molecular Biology and Evolution, 32(1), 268–274. https://doi.org/10.1093/molbev/msu300

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(4), 450–470. https://doi.org/10.1080/09670262.2014.976843

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(5), 976–996. https://doi.org/10.1111/JPY.12897

R Core Team. (2021). A language and environment for statistical computing. R Foundation for Statistical Computing. https://www.r‐project.org/

Ronquist, F., Teslenko, M., Van Der Mark, P., Ayres, D. L., Darling, A., Höhna, 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(3), 539–542. https://doi.org/10.1093/SYSBIO/SYS029

Skoupý, S., Stanojković, A., Casamatta, D. A., McGovern, C., Martinović, A., Jaskowiec, J., Konderlová, M., Dodoková, V., Mikesková, P., Jahodářová, E., Jungblut, A., van Schalkwyk, H., & Dvořák, P. (2024). Population genomics and morphological data bridge the centuries of cyanobacterial taxonomy along the continuum of microcoleus species. iScience, 27(4), 109444. https://doi.org/10.1016/j.isci.2024.109444

Skoupý, S., Stanojković, A., Pavlíková, M., Poulíčková, A., & Dvořák, P. (2022). New cyanobacterial genus Argonema is hiding in soil crusts around the world. Scientific Reports, 12(1), 7203. https://doi.org/10.1038/s41598‐022‐11288‐4

Stackebrandt, E., & Ebers, J. (2006). Taxonomic parameters revisited: Tarnished gold standards. Microbiology Today, 33, 152–155.

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(4), 846–849. https://doi.org/10.1099/00207713‐44‐4‐846

Stanojković, A., Skoupý, S., Johannesson, H., & Dvořák, P. (2024). The global speciation continuum of the cyanobacterium microcoleus. Nature Communications, 15(1), 2122. https://doi.org/10.1038/s41467‐024‐46459‐6

Stanojković, A., Skoupý, S., Škaloud, P., & Dvořák, P. (2022). High genomic differentiation and limited gene flow indicate recent cryptic speciation within the genus Laspinema (Cyanobacteria). Frontiers in Microbiology, 13, 977454. https://doi.org/10.3389/fmicb.2022.977454

Staub, R. (1961). Research on physiology of nutrients of the planktonic cyanobacterium Oscillatoria rubescens. Schweizerische Zeitschrift Fur Hydrologie, 23, 82–198.

Thompson, C. C., Chimetto, L., Edwards, R. A., Swings, J., Stackebrandt, E., & Thompson, F. L. (2013). Microbial genomic taxonomy. BMC Genomics, 14(1), 913. https://doi.org/10.1186/1471‐2164‐14‐913

Turner, S., Pryer, K. M., Miao, V. P. W., & Palmer, J. D. (1999). Investigating deep phylogenetic relationships among cyanobacteria and plastids by small subunit rRNA sequence Analysis. Journal of Eukaryotic Microbiology, 46(4), 327–338. https://doi.org/10.1111/J.1550‐7408.1999.TB04612.X

Willis, A., & Woodhouse, J. N. (2020). Defining cyanobacterial species: Diversity and description through genomics. Critical Reviews in Plant Sciences, 39(2), 101–124. https://doi.org/10.1080/07352689.2020.1763541

Wright, S. (1965). The interpretation of population structure by F‐statistics with special regard to Systems of Mating. Evolution, 19(3), 395–420. https://doi.org/10.1111/j.1558‐5646.1965.tb01731.x

Zimba, P. V., Shalygin, S., Huang, I. S., Momčilović, M., & Abdulla, H. (2021). A new boring toxin producer–Perforafilum tunnelli gen. & sp. nov. (Oscillatoriales, Cyanobacteria) isolated from Laguna Madre, Texas, USA. Phycologia, 60(1), 10–24. https://doi.org/10.1080/00318884.2020.1808389

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

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