The filamentous cyanobacterium Microcoleus is among the most important global primary producers, especially in hot and cold desert ecosystems. This taxon represents a continuum consisting of a minimum of 12 distinct species with varying levels of gene flow and divergence. The notion of a species continuum is poorly understood in most lineages but is especially challenging in cyanobacteria. Here we show that genomic diversification of the Microcoleus continuum is reflected by morphological adaptation. We compiled a dataset of morphological data from 180 cultured strains and 300 whole genome sequences, including eight herbarium specimens and the type specimen of Microcoleus. We employed a combination of phylogenomic, population genomic, and population-level morphological data analyses to delimit species boundaries. Finally, we suggest that the shape of the filament apices may have an adaptive function to environmental conditions in the soil.

Department of Biology College of Arts and Sciences University of North Florida 1 UNF Drive Jacksonville FL 32224 USA

Department of Biology Faculty of Education Palacký University Olomouc Purkrabská 2 771 40 Olomouc Czech Republic

Department of Botany Faculty of Science Palacký University Olomouc Šlechtitelů 27 783 71 Olomouc Czech Republic

Department of Science Natural History Museum Cromwell Road London SW7 5BD Great Britain

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Nelson C., Giraldo-Silva A., Warsop Thomas F., Garcia-Pichel F. Spatial self-segregation of pioneering cyanobacterial species drives microbiome organization in biocrusts. ISME Commun. 2022;2:114. doi: 10.1038/s43705-022-00199-0. PubMed DOI PMC

Garcia-Pichel F., Belnap J. Microenvironments and microscale productivity of cyanobacterial desert crusts. J. Phycol. 1996;32:774–782. doi: 10.1111/j.0022-3646.1996.00774.x. DOI

Rodriguez-Caballero E., Belnap J., Büdel B., Crutzen P.J., Andreae M.O., Pöschl U., Weber B. Dryland photoautotrophic soil surface communities endangered by global change. Nat. Geosci. 2018;11:185–189. doi: 10.1038/s41561-018-0072-1. DOI

Williams L., Borchhardt N., Colesie C., Baum C., Komsic-Buchmann K., Rippin M., Becker B., Karsten U., Büdel B. Biological soil crusts of Arctic Svalbard and of Livingston Island, Antarctica. Polar Biol. 2017;40:399–411. doi: 10.1007/s00300-016-1967-1. DOI

Garcia-Pichel F., Wojciechowski M.F. The evolution of a capacity to build supra-cellular ropes enabled filamentous cyanobacteria to colonize highly erodible substrates. PLoS One. 2009;4 doi: 10.1371/journal.pone.0007801. PubMed DOI PMC

Stanojković A., Skoupý S., Johannesson H., Dvořák P. The global speciation continuum of the cyanobacterium Microcoleus. Nat. Commun. 2024;15:2122. doi: 10.1038/s41467-024-46459-6. PubMed DOI PMC

Garcia-Pichel F., Prufert-Bebout L., Muyzer G. Phenotypic and phylogenetic analyses show Microcoleus chthonoplastes to be a cosmopolitan cyanobacterium. Appl. Environ. Microbiol. 1996;62:3284–3291. doi: 10.1128/aem.62.9.3284-3291.1996. PubMed DOI PMC

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

Doolittle W.F., Zhaxybayeva O. On the origin of prokaryotic species. Genome Res. 2009;19:744–756. doi: 10.1101/gr.086645.108. PubMed DOI

Baptiste E., Ómalley M.A., Beiko R.G., Ereshefsky M., Gogarten J.P., Franklin-Hall L., Lapointe F.J., Dupre J., Dagan T., Boucher Y., Martin W. Prokaryotic evolution and tree of life are two different things. Biol. Direct. 2009;4:34. doi: 10.1186/1745-6150-4-34. PubMed DOI PMC

Gonzalez J.M., Puerta-Fernández E., Santana M.M., Rekadwad B. On a Non-Discrete Concept of Prokaryotic Species. Microorganisms. 2020;8:1723. doi: 10.3390/microorganisms8111723. PubMed DOI PMC

Johnson E.A., Miyanishi K. Testing the assumptions of chronosequences in succession. Ecol. Lett. 2008;11:419–431. doi: 10.1111/j.1461-0248.2008.01173.x. PubMed DOI

White N.J., Snook R.R., Eyres I. The past and future of experimental speciation. Trends Ecol. Evol. 2020;35:10–21. doi: 10.1016/j.tree.2019.08.009. PubMed DOI

Shaw K.L., Mullen S.P. Speciation Continuum. J. Hered. 2014;105:741–742. doi: 10.1093/jhered/esu060. PubMed DOI

Stanowski S., Ravinet M. Defining the speciation continuum. Evolution. 2020;75–6:1256–1276. doi: 10.1111/evo.14215. PubMed DOI

Mayr E. Columbia Univ. Press; 1942. Systematics and the Origin of Species.

Coyne J.A., Orr H.A. Sinauer Associates; 2004. Speciation.

Bobay L.M. In: The Pangenome: Diversity, Dynamics and Evolution of Genomes. Tettelin H., Medini D., editors. Springer; 2020. The Prokaryotic Species Concept and Challenges. PubMed DOI

Bobay L.M., Ochman H. Biological species are universal across life’s domains. Genome Biol. Evol. 2017;9:491–501. doi: 10.1093/gbe/evx026. PubMed DOI PMC

Fraser C., Hanage W.P., Spratt B.G. Recombination and the nature of bacterial speciation. Science. 2007;315:476–480. doi: 10.1126/science.1127573. PubMed DOI PMC

Dvořák P., Jahodářová E., Stanojković A., Skoupý S., Casamatta D.A. Population genomics meets the taxonomy of cyanobacteria. Algal Res. 2023;72 doi: 10.1016/j.algal.2023.103128. DOI

Hohenlohe P.A., Hand B.K., Andrews K.R., Luikart G. In: Population Genomics. Population Genomics. Rajora O., editor. Springer; 2018. Population Genomics Provides Key Insights in Ecology and Evolution. DOI

Black W.C., 4th, Baer C.F., Antolin M.F., Du Teau N.M. Population genomics: genome-wide sampling of insect populations. Annu. Rev. Entomol. 2001;46:441–469. doi: 10.1146/annurev.ento.46.1.441. PubMed DOI

Luikart G., England P.R., Tallmon D., Jordan S., Taberlet P. The power and promise of population genomics: from genotyping to genome typing. Nat. Rev. Genet. 2003;4:981–994. doi: 10.1038/nrg1226. PubMed DOI

Kashtan N., Roggensack S.E., Rodrigue S., Thompson J.W., Biller S.J., Coe A., Ding H., Marttinen P., Malmstrom R.R., Stocker R., et al. Single-cell genomics reveals hundreds of coexisting subpopulations in wild Prochlorococcus. Science. 2014;344:416–420. doi: 10.1126/science.1248575. PubMed DOI

Stanojković A., Skoupý S., Hašler P., Poulíčková A., Dvořák P. Geography and climate drive the distribution and diversification of the cosmopolitan cyanobacterium Microcoleus (Oscillatoriales, Cyanobacteria) Eur. J. Phycol. 2022;57:396–405. doi: 10.1080/09670262.2021.2007420. DOI

Skoupý S., Stanojković A., Pavlíková M., Poulíčková A., Dvořák P. New cyanobacterial genus Argonema is hiding in soil crusts around the world. Sci. Rep. 2022;12:7203. doi: 10.1038/s41598-022-11288-4. PubMed DOI PMC

Komárek J. Recent Changes in Cyanobacteria Taxonomy Based on a Combination of Molecular Background with Phenotype and Ecological Consequences (Genus and Species Concept) Hydrobiologia. 2010;639:245–259. doi: 10.1007/s10750-009-0031-3. DOI

Casamatta D.A., Vis M.L., Sheath R.G. Cryptic species in cyanobacterial systematics: a case study of Phormidium retzii (Oscillatoriales) using 16S rDNA and RAPD analyses. Aquat. Bot. 2003;77:295–309. doi: 10.1016/j.aquabot.2003.08.005. DOI

Jahodářová E., Dvořák P., Hašler P., Holušová K., Poulíčková A. Elainella gen. nov.: a new tropical cyanobacterium characterized using a complex genomic approach. Eur. J. Phycol. 2018;53:39–51. doi: 10.1080/09670262.2017.1362591. DOI

Nevill P.G., Zhong X., Tonti-Filippini J., Byrne M., Hislop M., Thiele K., van Leeuwen S., Boykin L.M., Small I. Large scale genome skimming for herbarium material for accurate plant identification and phylogenomics. Plant Methods. 2020;16:1. doi: 10.1186/s13007-019-0534-5. PubMed DOI PMC

Swali P., Schulting R., Gilardet A., Kelly M., Anastasiadou K., GLocke I., McCabe J., Williams M., Audsley T., Loe L., et al. Yersinia pestis genomes reveal plague in Britain 4000 years ago. Nat. Commun. 2023;14:2930. doi: 10.1038/s41467-023-38393-w. PubMed DOI PMC

Dvořák P., Hašler P., Poulíčková A. New insights into the genomic evolution of cyanobacteria using herbarium exsiccate. Eur. J. Phycol. 2020;55:30–38. doi: 10.1080/09670262.2019.1638523. DOI

Jungblut A.D., Raymond F., Dion M.B., Moineau S., Mohit V., Nguyen G.Q., Déraspe M., Francovic-Fontaine É., Lovejoy C., Culley A.I., et al. Genomic diversity and CRISPR-Cas systems in the cyanobacterium Nostoc in the High Arctic. Environ. Microbiol. 2021;23:2955–2968. doi: 10.1111/1462-2920.15481. PubMed DOI

Zhang C., Rabiee M., Sayyari E., Mirarab S. ASTRAL-III: polynomial time species tree reconstruction from partially resolved gene trees. BMC Bioinf. 2018;19:153. doi: 10.1186/s12859-018-2129-y. PubMed DOI PMC

Croucher N.J., Page A.J., Connor T.R., Delaney A.J., Keane J.A., Bentley S.D., Parkhill J., Harris S.R. Rapid phylogenetic analysis of large samples of recombinant bacterial whole genome sequences using Gubbins. Nucleic Acids Res. 2015;43:e15. doi: 10.1093/nar/gku1196. PubMed DOI PMC

Kollár J., Poulíčková A., Dvořák P. On the relativity of species, or the probabilistic solution to the species problem. Mol. Ecol. 2022;31:411–418. doi: 10.1111/mec.16218. PubMed DOI

Hanage W.P. Fuzzy species revisited. BMC Biol. 2013;11:41. doi: 10.1186/1741-7007-11-41. PubMed DOI PMC

Johansen J.R., Mareš J., Pietrasiak N., Bohunická M., Zima J., Štenclová L., Hauer T. Highly divergent 16S rRNA sequences in ribosomal operons of Scytonema hyalinum (Cyanobacteria) PLoS One. 2017;12 doi: 10.1371/journal.pone.0186393E. PubMed DOI PMC

Casamatta D.A., Villanueva C.D., Garvey A.D., Stocks H.S., Vaccarino M., Dvořák P., Hašler P., Johansen J.R. Reptodigitus Chapmanii (Nostocales, Hapalosiphonaceae) Gen. Nov.: A Unique Nostocalean (Cyanobacteria) Genus Based on a Polyphasic Approach. J. Phycol. 2020;56:425–436. doi: 10.1111/jpy.12954. PubMed DOI

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

Smith G.R. Homologous recombination in prokaryotes: enzymes and controlling sites. Genome. 1989;31:520–527. doi: 10.1139/g89-100. PubMed DOI

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

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

Osorio-Santos K., Pietrasiak N., Bohunická M., Miscoe L.H., Kováčik L., Martin M.P., Bohunická M. Seven new species of Oculatella (Pseudanabaenales, Cyanobacteria): taxonomically recognizing cryptic diversification. Eur. J. Phycol. 2014;49:450–470. doi: 10.1080/09670262.2014.976843. DOI

Komárek J. Quo vadis, taxonomy of cyanobacteria. Fottea. 2020;20:104–110. doi: 10.5507/fot.2019.020. DOI

Komárek J. Cyanobacterial taxonomy: current problems and prospects for the integration of traditional and molecular approaches. ALGAE. 2006;21:349–375. doi: 10.4490/algae.2006.21.4.349. DOI

Koch R., Kupczok A., Stucken K., Ilhan J., Hammerschmidt K., Dagan T. Plasticity first: Molecular signatures of a complex morphological trait in filamentous cyanobacteria. BMC Evol. Biol. 2017;17 doi: 10.1186/s12862-017-1053-5. PubMed DOI PMC

Pietrasiak N., Reeve S., Osorio-Santos K., Lipson D.A., Johansen J.R. Trichotorquatus gen. nov. - a new genus of soil cyanobacteria discovered from American drylands. J. Phycol. 2021;57:886–902. doi: 10.1111/jpy.13147. PubMed DOI

Colombi T., Kirchgessner N., Walter A., Keller T. Root tip shape governs root elongation rate under increased soil strength. Plant Physiol. 2017;174:2289–2301. doi: 10.1104/pp.17.00357. PubMed DOI PMC

Abdirad S., Ghaffari M.R., Majd A., Irian S., Soleymaniniya A., Daryani P., Koobaz P., Shobbar Z.S., Farsad L.K., Yazdanpanah P., et al. Genome-Wide Expression Analysis of Root Tips in Contrasting Rice Genotypes Revealed Novel Candidate Genes for Water Stress Adaptation. Front. Plant Sci. 2022;13:792079. doi: 10.3389/fpls.2022.792079. PubMed DOI PMC

Perkerson Iii R.B., Johansen J.R., Kovácik L., Brand J., Kaštovský J., Casamatta D.A. A unique Pseudanabaenalean (Cyanobacteria) genus Nodosilinea gen. nov. based on morphological and molecular data. J. Phycol. 2011;47:1397–1412. doi: 10.1111/j.1529-8817.2011.01077.x. PubMed DOI

Komárek J., Anagnostidis K. In: Süβwasserflora von MItteleuropa. Büdel B., Krienitz L., Gärtner G., Schagerl M., editors. Elsevier GmbH; 2005. Cyanoprokaryota 2nd Part: Oscillatoriales.

Beck J.B., Semple J.C. Next-generation sampling: Pairing genomics with herbarium specimens provides species-level signal in Solidago (Asteraceae) Appl. Plant Sci. 2015;3 doi: 10.3732/apps.1500014[. PubMed DOI PMC

Drouet F. The academy of Natural Sciences of Philadelphia, Fulton Press Inc; 1968. Revision of the Classification of the Oscillatoriaceae.

Gomont M. Vol. 15. Annales des Sciences Naturelles, Botanique; 1892. pp. 263–368. (Monographie des Oscillariées (Nostocacées homocystées)).

Churro C., Semedo-Aguiar A.P., Silva A.D., Pereira-Leal J.B., Leite R.B. A novel cyanobacterial geosmin producer, revising GeoA distribution and dispersion patterns in Bacteria. Sci. Rep. 2020;10:8679. doi: 10.1038/s41598-020-64774-y. PubMed DOI PMC

Mishler B.D. In: Species Problem and Beyond, Contemporary Issue in Philosophy and Practice. Wilkins J.S., Zachos F.E., Pavlinov I.Y., editors. CRC Press; 2022. Ecology, Evolution and Systematics in a Post-Species world.

Wilkins J.S. How to be a chaste species pluralist-realist: The origins of species modes and the synapomorphies species concept. Biol. Philos. 2003;18:621–638. doi: 10.1023/A:1026390327482. DOI

Haber M.H. Species in the age of discordance. Philos. Theor. Pract. Biol. 2019;11:21.

Quinn A. In: Species Problems and Beyond, Contemporary Issues in Philosophy and Practice. Wilkins J.S., Zachos F.E., Pavlinov I.Y., editors. CRC Press; 2022. Species in the Time of Big Data: The multi-Species Coalescent, the General Lineage Concept, and Species Delimitation.

Smith M.L., Carstens B.C. In: Species Problems and Beyond, Contemporary Issues in Philosophy and Practice. Wilkins J.S., Zachos F.E., Pavlinov I.Y., editors. CRC Press; 2022. Species Delimitation Using Molecular Data.

Kollár J., Poulíčková A., Dvořák P. On the relativity of species, or the probabilistic solution to the species problem. Mol. Ecol. 2022;31:411–418. doi: 10.1111/mec.16218. PubMed DOI

Staub R. Ernährungsphysiologisch-autökologische Untersuchungen an der planktischen Blaualge Oscillatoria rubescens DC. ETH Zürich. 1961 doi: 10.3929/ethz-a-000092335. DOI

Emms D.M., Kelly S. OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biol. 2019;20:238. doi: 10.1186/s13059-019-1832-y. PubMed DOI PMC

Nguyen L.T., Schmidt H.A., von Haeseler A., Minh B.Q. IQ-TREE: A fast and effective stochastic algorithm for estimating maximum likelihood phylogenies. Mol. Biol. Evol. 2015;32:268–274. doi: 10.1093/molbev/msu300. PubMed DOI PMC

Tonkin-Hill G., Lees J.A., Bentley S.D., Frost S.D.W., Corander J. Fast hierarchical Bayesian analysis of population structure. Nucleic Acids Res. 2019;47:5539–5549. doi: 10.1093/nar/gkz361. PubMed DOI PMC

R Core Team . R Foundation for Statistical Com-puting; 2022. R: A Language and Environment for Statistical Compu-ting.https://www.R-project.org/

Larsson A. AliView: a fast and lightweight alignment viewer and editor for large data sets. Bioinformatics. 2014;30:3276–3278. doi: 10.1093/bioinformatics/btu531. PubMed DOI PMC

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

Singh J., Hanson J., Paliwal K., Zhou Y. RNA secondary structure prediction using an ensemble of two-dimensional deep neural networks and transfer learning. Nat. Commun. 2019;10 doi: 10.1038/s41467-019-13395-9. PubMed DOI PMC

Hammer Ø., Harper D.A., Ryan P.D. Past: Paleontological Statistics Software Package For Education And Data Analysis. Paleontologia Electronica. 2001;4:1–9. http://palaeo-electronica.org/2001_1/past/issue1_01.htm

QGIS.org, %Y . QGIS Association; 2021. QGIS Geographic Information System.http://www.qgis.org

Hašler P., Dvořák P., Johansen J.R., Kitner M., Ondřej V., Poulíčková A. Morphological and molecular study of epipelic filamentous genera Phormidium, Microcoleus and Geitlerinema (Oscillatoriales, Cyanophyta/Cyanobacteria) Fottea. 2012;12:341–356. doi: 10.5507/fot.2012.024. DOI

Stanojković A., Skoupý S., Škaloud P., Dvořák P. High genomic differentiation and limited gene flow indicate recent cryptic speciation within the genus Laspinema (cyanobacteria) Front. Microbiol. 2022;13 doi: 10.3389/fmicb.2022.977454. PubMed DOI PMC

Dvořák P., Jahodářová E., Casamatta D.A., Hašler P., Poulíčková A. Difference without distinction? Gaps in cyanobacterial systematics; when more is just too much. Fottea. 2018;18:130–136. doi: 10.5507/fot.2017.023. DOI

Edgar R.C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32:1792–1797. doi: 10.1093/nar/gkh340. PubMed DOI PMC

Kalyaanamoorthy S., Minh B.Q., Wong T.K.F., von Haeseler A., Jermiin L.S. ModelFinder: Fast Model Selection for Accurate Phylogenetic Estimates. Nat. Methods. 2017;14:587–589. doi: 10.1038/nmeth.4285. PubMed DOI PMC

Fick S.E., Hijmans R.J. WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas. Int. J. Climatol. 2017;37:4302–4315. doi: 10.1002/joc.5086. DOI

McDowell R.W., Noble A., Pletnyakov P., Haygarth P.M. A Global Database of Soil Plant Available Phosphorus. Sci. Data. 2023;10:e125. doi: 10.1038/s41597-023-02022-4. PubMed DOI PMC

Beckmann M., Václavík T., Manceur A.M., Šprtová L., Von Wehrden H., Welk E., Cord A.F. glUV: a global UV-B radiation data set for macroecological studies. Methods Ecol. Evol. 2014;5:372–383. doi: 10.1111/2041-210X.12168. DOI

Haberl H., Erb K.H., Krausmann F., Gaube V., Bondeau A., Plutzar C., Gingrich S., Lucht W., Fischer-Kowalski M. Quantifying and mapping the human appropriation of net primary production in earth’s terrestrial ecosystems. Proc. Natl. Acad. Sci. USA. 2007;104:12942–12947. doi: 10.1073/pnas.0704243104. PubMed DOI PMC