In this study, we used microscopic, spectroscopic, and molecular analysis to characterize endolithic colonization in gypsum (selenites and white crystalline gypsum) from several sites in Sicily. Our results showed that the dominant microorganisms in these environments are cyanobacteria, including: Chroococcidiopsis sp., Gloeocapsopsis pleurocapsoides, Gloeocapsa compacta, and Nostoc sp., as well as orange pigmented green microalgae from the Stephanospherinia clade. Single cell and filament sequencing coupled with 16S rRNA amplicon metagenomic profiling provided new insights into the phylogenetic and taxonomic diversity of the endolithic cyanobacteria. These organisms form differently pigmented zones within the gypsum. Our metagenomic profiling also showed differences in the taxonomic composition of endoliths in different gypsum varieties. Raman spectroscopy revealed that carotenoids were the most common pigments present in the samples. Other pigments such as gloeocapsin and scytonemin were also detected in the near-surface areas, suggesting that they play a significant role in the biology of endoliths in this environment. These pigments can be used as biomarkers for basic taxonomic identification, especially in case of cyanobacteria. The findings of this study provide new insights into the diversity and distribution of phototrophic microorganisms and their pigments in gypsum in Southern Sicily. Furthemore, this study highlights the complex nature of endolithic ecosystems and the effects of gypsum varieties on these communities, providing additional information on the general bioreceptivity of these environments.

Center Algatech Institute of Microbiology The Czech Academy of Sciences Třeboň Czechia

Department of Biochemistry and Microbial Ecology Museo Nacional de Ciencias Naturales Consejo Superior de Investigaciones Científicas Madrid Spain

Department of Earth and Planetary Science University of Berkeley Berkeley CA United States

Department of Ecology Faculty of Science Charles University Prague Czechia

Department of Parasitology Faculty of Science University of South Bohemia České Budějovice Czechia

Innovative Genomics Institute University of California Berkeley Berkeley CA United States

Institute of Experimental and Applied Physics Czech Technical University Prague Prague Czechia

Institute of Geochemistry Mineralogy and Mineral Resources Faculty of Science Charles University Prague Czechia

Institute of Hydrobiology Biology Centre of the Czech Academy of Sciences České Budějovice Czechia

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Águila B., Alcántara-Hernández R. J., Montejano G., López-Martínez R., Falcón L. I., Becerra-Absalón I. (2021). Cyanobacteria in microbialites of Alchichica Crater Lake: a polyphasic characterization. Eur. J. Phycol. 56, 428–443. doi: 10.1080/09670262.2020.1853815 DOI

Al-Wakeel E.-S. I. (2002). Alabaster, and selenite gypsum: I-dehydration-rehydration comparison studies. J. Mater. Res. Technol. 18, 365–368.

Andrews S. (2010). FastQC: a quality control tool for high throughput sequence data. Available at: http://www.bioinformatics.babraham.ac.uk/projects/fastqc

Archer S. D., de los Ríos A., Lee K. C., Niederberger T. S., Cary S. C., Coyne K. J., et al. . (2017). Endolithic microbial diversity in sandstone and granite from the McMurdo Dry Valleys, Antarctica. Polar Biol. 40, 997–1006. doi: 10.1007/s00300-016-2024-9 DOI

Ascaso C., Wierzchos J., Souza-Egipsy V., Delosrios A., Rodrigues J. (2002). In situ evaluation of the biodeteriorating action of microorganisms and the effects of biocides on carbonate rock of the Jeronimos Monastery (Lisbon). Int. Biodeterior. Biodegrad. 49, 1–12. doi: 10.1016/S0964-8305(01)00097-X DOI

Bahl J., Lau M. C., Smith G. J., Vijaykrishna D., Cary S. C., Lacap D. C., et al. . (2011). Ancient origins determine global biogeography of hot and cold desert cyanobacteria. Nat. Commun. 2, 163–166. doi: 10.1038/ncomms1167, PMID: PubMed DOI PMC

Balskus E. P., Case R. J., Walsh C. T. (2011). The biosynthesis of cyanobacterial sunscreen scytonemin in intertidal microbial mat communities. FEMS Microbiol. Ecol. 77, 322–332. doi: 10.1111/j.1574-6941.2011.01113.x, PMID: PubMed DOI PMC

Basilone L. (2018). Lithostratigraphy of Sicily. Cham: Springer.

Benison K. C., Karmanocky III F. J. (2014). Could microorganisms be preserved in Mars gypsum? Insights from terrestrial examples. Geology 42, 615–618. doi: 10.1130/G35542.1 DOI

Bowers R. M., Nayfach S., Schulz F., Jungbluth S. P., Ruhl I. A., Sheremet A., et al. . (2022). Dissecting the dominant hot spring microbial populations based on community-wide sampling at single-cell genomic resolution. ISME J. 16, 1337–1347. doi: 10.1038/s41396-021-01178-4, PMID: PubMed DOI PMC

Brown J. J., Rodríguez-Ruano S. M., Poosakkannu A., Batani G., Schmidt J. O., Roachell W., et al. . (2020). Ontogeny, species identity, and environment dominate microbiome dynamics in wild populations of kissing bugs (Triatominae). Microbiome 8, 146–116. doi: 10.1186/s40168-020-00921-x, PMID: PubMed DOI PMC

Callahan B. J., McMurdie P. J., Rosen M. J., Han A. W., Johnson A. J. A., Holmes S. P. (2016). DADA2: high-resolution sample inference from Illumina amplicon data. Nat. Methods 13, 581–583. doi: 10.1038/nmeth.3869, PMID: PubMed DOI PMC

Caruso A., Pierre C., Blanc-Valleron M.-M., Rouchy J.-M. (2015). Carbonate deposition and diagenesis in evaporitic environments: the evaporative and Sulphur-bearing limestones during the settlement of the Messinian salinity crisis in Sicily and Calabria. Palaeogeogr. Palaeoclimatol. Palaeoecol. 429, 136–162. doi: 10.1016/j.palaeo.2015.03.035 DOI

Cho S. M., Kim S., Cho H., Lee H., Lee J. H., Lee H., et al. . (2019). Type II ice-binding proteins isolated from an arctic microalga are similar to adhesin-like proteins and increase freezing tolerance in transgenic plants. Plant Cell Physiol. 60, 2744–2757. doi: 10.1093/pcp/pcz162, PMID: PubMed DOI

Collins A. M., Jones H. D., Han D., Hu Q., Beechem T. E., Timlin J. A. (2011). Carotenoid distribution in living cells of Haematococcus pluvialis (Chlorophyceae). PLoS One 6:e24302. doi: 10.1371/journal.pone.0024302 PubMed DOI PMC

Crits-Christoph A., Robinson C. K., Ma B., Ravel J., Wierzchos J., Ascaso C., et al. . (2016). Phylogenetic and functional substrate specificity for endolithic microbial communities in hyper-arid environments. Front. Microbiol. 7:301. doi: 10.3389/fmicb.2016.00301, PMID: PubMed DOI PMC

Culka A., Osterrothová K., Hutchinson I., Ingley R., McHugh M., Oren A., et al. . (2014). Detection of pigments of halophilic endoliths from gypsum: Raman portable instrument and European Space Agency’s prototype analysis. Philos. Trans. A Math. Phys. Eng. Sci. 372:20140203. doi: 10.1098/rsta.2014.0203, PMID: PubMed DOI PMC

Cumbers J., Rothschild L. J. (2014). Salt tolerance and polyphyly in the cyanobacterium Chroococcidiopsis (Pleurocapsales). J. Phycol. 50, 472–482. doi: 10.1111/jpy.12169, PMID: PubMed DOI

Davey M. P., Norman L., Sterk P., Huete-Ortega M., Bunbury F., Loh B. K. W., et al. . (2019). Snow algae communities in Antarctica: metabolic and taxonomic composition. New Phytol. 222, 1242–1255. doi: 10.1111/nph.15701, PMID: PubMed DOI PMC

De los Ríos A., Cámara B., Del Cura M. A. G., Rico V. J., Galván V., Ascaso C. (2009). Deteriorating effects of lichen and microbial colonization of carbonate building rocks in the Romanesque churches of Segovia (Spain). Sci. Total Environ. 407, 1123–1134. doi: 10.1016/j.scitotenv.2008.09.042 PubMed DOI

de Oliveira V. E., Castro H. V., Edwards H. G. M., de Oliveira L. F. C. (2010). Carotenes and carotenoids in natural biological samples: a Raman spectroscopic analysis. J. Raman Spectrosc. 41, 642–650. doi: 10.1002/jrs.2493 DOI

Dillon J. G., Tatsumi C. M., Tandingan P. G., Castenholz R. W. (2002). Effect of environmental factors on the synthesis of scytonemin, a UV-screening pigment, in a cyanobacterium (Chroococcidiopsis sp.). Arch. Microbiol. 177, 322–331. doi: 10.1007/s00203-001-0395-x PubMed DOI

Edgar R. C. (2013). UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10, 996–998. doi: 10.1038/nmeth.2604 PubMed DOI

Edwards H. G. M., Garcia-Pichel F., Newton E., Wynn-Williams D. (2000). Vibrational Raman spectroscopic study of scytonemin, the UV-protective cyanobacterial pigment. Spectrochim. Acta A Mol. Biomol. Spectrosc. 56, 193–200. doi: 10.1016/s1386-1425(99)00218-8 PubMed DOI

Edwards H. G. M., Hutchinson I. B., Ingley R., Jehlička J. (2014). Biomarkers and their Raman spectroscopic signatures: a spectral challenge for analytical astrobiology. Philos. Trans. A Math. Phys. Eng. Sci. 372:20140193. doi: 10.1098/rsta.2014.0193 PubMed DOI

Ekebergh A., Sandin P., Mårtensson J. (2015). On the photostability of scytonemin, analogues thereof and their monomeric counterparts. Photochem. Photobiol. Sci. 14, 2179–2186. doi: 10.1039/C5PP00215J, PMID: PubMed DOI

Ertekin E., Meslier V., Browning A., Treadgold J., DiRuggiero J. (2020). Rock structure drives the taxonomic and functional diversity of endolithic microbial communities in extreme environments. Environ. Microbiol. 23, 3937–3956. doi: 10.1111/1462-2920.15287, PMID: PubMed DOI

Ferris F., Lowson E. (1997). Ultrastructure and geochemistry of endolithic microorganisms in limestone of the Niagara escarpment. Can. J. Microbiol. 43, 211–219. doi: 10.1139/m97-029 DOI

Friedmann E. I. (1982). Endolithic microorganisms in the Antarctic cold desert. Science 215, 1045–1053. doi: 10.1126/science.215.4536.1045, PMID: PubMed DOI

Friedmann I., Lipkin Y., Ocampo-Paus R. (1967). Desert algae of the Negev (Israel). Phycologia 6, 185–200. doi: 10.2216/i0031-8884-6-4-185.1 DOI

Gálvez F. E., Saldarriaga-Córdoba M., Huovinen P., Silva A. X., Gómez I. (2021). Revealing the characteristics of the Antarctic snow alga Chlorominima collina gen. et sp. nov. through taxonomy, physiology, and transcriptomics. Front. Plant Sci. 12:662298. doi: 10.3389/fpls.2021.662298, PMID: PubMed DOI PMC

Gao X. (2017). Scytonemin plays a potential role in stabilizing the exopolysaccharidic matrix in terrestrial cyanobacteria. Microb. Ecol. 73, 255–258. doi: 10.1007/s00248-016-0851-4 PubMed DOI

Garcia-Pichel F., Castenholz R. W. (1991). Characterization and biological implications of scytonemin, a cyanobacterial sheath pigment. J. Phycol. 27, 395–409. doi: 10.1111/j.0022-3646.1991.00395.x DOI

García-Veigas J., Cendón D. I., Gibert L., Lowenstein T. K., Artiaga D. (2018). Geochemical indicators in Western Mediterranean Messinian evaporites: implications for the salinity crisis. Mar. Geol. 403, 197–214. doi: 10.1016/j.margeo.2018.06.005 DOI

Golubic S., Friedmann E. I., Schneider J. (1981). The lithobiontic ecological niche, with special reference to microorganisms. J. Sediment. Res. 51, 475–478. doi: 10.1306/212F7CB6-2B24-11D7-8648000102C1865D DOI

Gorbushina A. A. (2007). Life on the rocks. Environ. Microbiol. 9, 1613–1631. doi: 10.1111/j.1462-2920.2007.01301.x PubMed DOI

Grant C. S., Louda J. W. (2013). Scytonemin-imine, a mahogany-colored UV/Vis sunscreen of cyanobacteria exposed to intense solar radiation. Org. Geochem. 65, 29–36. doi: 10.1016/j.orggeochem.2013.09.014 DOI

Grünewald K., Hirschberg J., Hagen C. (2001). Ketocarotenoid biosynthesis outside of plastids in the unicellular green alga Haematococcus pluvialis. J. Biol. Chem. 276, 6023–6029. doi: 10.1074/jbc.M006400200, PMID: PubMed DOI

Horath T., Neu T., Bachofen R. (2006). An endolithic microbial community in dolomite rock in Central Switzerland: characterization by reflection spectroscopy, pigment analyses, scanning electron microscopy, and laser scanning microscopy. Microb. Ecol. 51, 353–364. doi: 10.1007/s00248-006-9051-y, PMID: PubMed DOI

Jehlička J., Culka A., Mareš J. (2019). Raman spectroscopic screening of cyanobacterial chasmoliths from crystalline gypsum—the Messinian crisis sediments from Southern Sicily. J. Raman Spectrosc. 51, 1802–1812. doi: 10.1002/jrs.5671 DOI

Jehlička J., Culka A., Nedbalová L. (2016). Colonization of snow by microorganisms as revealed using miniature Raman spectrometers—possibilities for detecting carotenoids of psychrophiles on Mars? Astrobiology 16, 913–924. doi: 10.1089/ast.2016.1487, PMID: PubMed DOI

Jehlička J., Edwards H. G. M., Oren A. (2014a). Raman spectroscopy of microbial pigments. Appl. Environ. Microbiol. 80, 3286–3295. doi: 10.1128/AEM.00699-14, PMID: PubMed DOI PMC

Jehlička J., Edwards H. G. M., Osterrothová K., Novotná J., Nedbalová L., Kopecký J., et al. . (2014b). Potential and limits of Raman spectroscopy for carotenoid detection in microorganisms: implications for astrobiology. Philos. Trans. A Math. Phys. Eng. Sci. 372:20140199. doi: 10.1098/rsta.2014.0199, PMID: PubMed DOI PMC

Johansen J. R., Hentschke G. S., Pietrasiak N., Rigonato J., Fiore 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. doi: 10.5507/fot.2017.002 DOI

Jung W., Campbell R. L., Gwak Y., Kim J. I., Davies P. L., Jin E. (2016). New cysteine-rich ice-binding protein secreted from Antarctic microalga, Chloromonas sp. PLoS One 11:e0154056. doi: 10.1371/journal.pone.0154056, PMID: PubMed DOI PMC

Katoh K., Standley D. M. (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772–780. doi: 10.1093/molbev/mst010, PMID: PubMed DOI PMC

Komárek J. (2013). “Cyanoprokaryota: 3rd part: heterocystous genera” in Süßwasserflora von Mitteleuropa, Bd 19 (3). eds. Büdel B., Gärtner G., Krienitz L., Schagerl M. (Berlin: Springer Spektrum; ), 1–1130.

Komárek J. (2016). A polyphasic approach for the taxonomy of cyanobacteria: principles and applications. Eur. J. Phycol. 51, 346–353. doi: 10.1080/09670262.2016.1163738 DOI

Komárek J., Anagnostidis K. (1999). “Cyanoprokaryota. I. Chroococcales” in Süßwasserflora von Mitteleuropa, Begründet von A. PascherBd, 19/3 Cyanoprokaryota, 1. Teil Chroococcales. eds. Ettl H., Gärtner G., Heynig H., Mollenhauer D. (Heidelberg: Spektrum Akademischer Verlag; ), 1–548.

Komárek J., Anagnostidis K. (2005). “Cyanoprokaryota. 2. Teil: Oscillatoriales” in Süßwasserflora von Mitteleuropa, Bd 19 (2). eds. Büdel B., Gärtner G., Krienitz L., Schagerl M. (München: Elsevier GmbH; ), 1–759.

Kurmayer R., Christiansen G., Holzinger A., Rott E. (2018). Single colony genetic analysis of epilithic stream algae of the genus Chamaesiphon spp. Hydrobiologia 811, 61–75. doi: 10.1007/s10750-017-3295-z, PMID: PubMed DOI PMC

Kuzmany H. (1980). Resonance Raman scattering from neutral and doped polyacetylene. Phys. Stat. Solid. B 97, 521–531. doi: 10.1002/pssb.2220970217 DOI

Lamprinou V., Hernández-Mariné M., Canals T., Kormas K., Economou-Amilli A., Pantazidou A. (2011). Morphology and molecular evaluation of Iphinoe spelaeobios gen. nov., sp. nov. and Loriellopsis cavernicola gen. nov., sp. nov., two stigonematalean cyanobacteria from Greek and Spanish caves. Int. J. Syst. Evol. Microbiol. 61, 2907–2915. doi: 10.1099/ijs.0.029223-0, PMID: PubMed DOI

Lara Y. J., McCann A., Malherbe C., François C., Demoulin C. F., Sforna M. C., et al. . (2022). Characterization of the halochromic Gloeocapsin pigment, a cyanobacterial biosignature for paleobiology and astrobiology. Astrobiology 22, 735–754. doi: 10.1089/ast.2021.0061, PMID: PubMed DOI

Maguregui M., Knuutinen U., Trebolazabala J., Morillas H., Castro K., Martinez-Arkarazo I., et al. . (2012). Use of in situ and confocal Raman spectroscopy to study the nature and distribution of carotenoids in brown patinas from a deteriorated wall painting in Marcus Lucretius house (Pompeii). Anal. Bioanal. Chem. 402, 1529–1539. doi: 10.1007/s00216-011-5276-9 PubMed DOI

Mareš J., Hrouzek P., Kaňa R., Ventura S., Strunecký O., Komárek J. (2013). The primitive thylakoid-less cyanobacterium Gloeobacter is a common rock-dwelling organism. PLoS One 8:e66323. doi: 10.1371/journal.pone.0066323, PMID: PubMed DOI PMC

Mareš J., Lara Y., Dadáková I., Hauer T., Uher B., Wilmotte A., et al. . (2015). Phylogenetic analysis of cultivation-resistant terrestrial cyanobacteria with massive sheaths (Stigonema spp. and Petalonema alatum, Nostocales, Cyanobacteria) using single-cell and filament sequencing of environmental samples. J. Phycol. 51, 288–297. doi: 10.1111/jpy.12273 PubMed DOI

Marotz C., Sharma A., Humphrey G., Gottel N., Daum C., Gilbert J. A., et al. . (2019). Triplicate PCR reactions for 16S rRNA gene amplicon sequencing are unnecessary. Biotechniques 67, 29–32. doi: 10.2144/btn-2018-0192, PMID: PubMed DOI PMC

Matsuzaki R., Kawai-Toyooka H., Hara Y., Nozaki H. (2015). Revisiting the taxonomic significance of aplanozygote morphologies of two cosmopolitan snow species of the genus Chloromonas (Volvocales, Chlorophyceae). Phycologia 54, 491–502. doi: 10.2216/15-33.1 DOI

McMurdie P. J., Holmes S. (2013). Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 8:e61217. doi: 10.1371/journal.pone.0061217, PMID: PubMed DOI PMC

Meslier V., Casero M. C., Dailey M., Wierzchos J., Ascaso C., Artieda O., et al. . (2018). Fundamental drivers for endolithic microbial community assemblies in the hyperarid Atacama Desert. Environ. Microbiol. 20, 1765–1781. doi: 10.1111/1462-2920.14106, PMID: PubMed DOI

Miscoe L. H., Johansen J. R., Kociolek J. P., Lowe R. L., Vaccarino M. A., Pietrasiak N., et al. . (2016). The diatom flora and cyanobacteria from caves on Kauai, Hawaii. Acta Bot. Hung. 58, 3–4.

Nedbalová L., Mihál M., Kvíderová J., Procházková L., Řezanka T., Elster J. (2017). Identity, ecology and ecophysiology of planktic green algae dominating in ice-covered lakes on James Ross island (northeastern Antarctic peninsula). Extremophiles 21, 187–200. doi: 10.1007/s00792-016-0894-y, PMID: PubMed DOI

Němečková K., Culka A., Jehlička J. (2022). Detecting pigments from gypsum endoliths using Raman spectroscopy: from field prospection to laboratory studies. J. Raman Spectrosc. 53, 630–644. doi: 10.1002/jrs.6144 DOI

Němečková K., Culka A., Němec I., Edwards H. G. M., Mareš J., Jehlička J. (2021). Raman spectroscopic search for scytonemin and gloeocapsin in endolithic colonizations in large gypsum crystals. J. Raman Spectrosc. 52, 2633–2647. doi: 10.1002/jrs.6186 DOI

Němečková K., Jehlička J., Culka A. (2020). Fast screening of carotenoids of gypsum endoliths using portable Raman spectrometer (Messinian gypsum, Sicily). J. Raman Spectrosc. 51, 1127–1137. doi: 10.1002/jrs.5891 DOI

Oksanen J. (2009). Vegan: Community ecology package. R package version 1.15–14. Available at: http://CRAN.R-project.org/package=vegan.

Orellana G., Gómez-Silva B., Urrutia M., Galetović A. (2020). UV-A irradiation increases Scytonemin biosynthesis in Cyanobacteria inhabiting halites at Salar Grande, Atacama Desert. Microorganisms 8:1690. doi: 10.3390/microorganisms8111690, PMID: PubMed DOI PMC

Osterrothová K., Culka A., Němečková K., Kaftan D., Nedbalová L., Procházková L., et al. . (2019). Analyzing carotenoids of snow algae by Raman microspectroscopy and high-performance liquid chromatography. Spectrochim. Acta A Mol. Biomol. Spectrosc. 212, 262–271. doi: 10.1016/j.saa.2019.01.013, PMID: PubMed DOI

Parada A. E., Needham D. M., Fuhrman J. A. (2016). Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environ. Microbiol. 18, 1403–1414. doi: 10.1111/1462-2920.13023 PubMed DOI

Pitonzo B. J., Amy P. S., Rudin M. (1999). Effect of gamma radiation on native endolithic microorganisms from a radioactive waste deposit site. Radiat. Res. 152, 64–70. doi: 10.2307/3580050, PMID: PubMed DOI

Posada D. (2008). jModelTest: phylogenetic model averaging. Mol. Biol. Evol. 25, 1253–1256. doi: 10.1093/molbev/msn083, PMID: PubMed DOI

Procházková L., Leya T., Křížková H., Nedbalová L. (2019). Sanguina nivaloides and Sanguina aurantia gen. et spp. nov. (Chlorophyta): the taxonomy, phylogeny, biogeography and ecology of two newly recognised algae causing red and orange snow. FEMS Microbiol. Ecol. 95:fiz064. doi: 10.1093/femsec/fiz064, PMID: PubMed DOI PMC

Quast C., Pruesse E., Yilmaz P., Gerken J., Schweer T., Yarza P., et al. . (2012). The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41, D590–D596. doi: 10.1093/nar/gks1219, PMID: PubMed DOI PMC

Rhind T., Ronholm J., Berg B., Mann P., Applin D., Stromberg J., et al. . (2014). Gypsum-hosted endolithic communities of the Lake St. Martin impact structure, Manitoba, Canada: spectroscopic detectability and implications for Mars. Int. J. Astrobiol. 13, 366–377. doi: 10.1017/S1473550414000378 DOI

R Core Team . (2021). R: A language and environment for statistical computing. Vienna, Austria. Available at: http://www.R-project.org/

Rstudio Team . (2021). RStudio: Integrated Development Environment for R. Boston, MA. Available at: http://www.rstudio.com/

Rott E., Holzinger A., Gesierich D., Kofler W., Sanders D. (2010). Cell morphology, ultrastructure, and calcification pattern of Oocardium stratum, a peculiar lotic desmid. Protoplasma 243, 39–50. doi: 10.1007/s00709-009-0050-y, PMID: PubMed DOI

Sanmartín P., DeAraujo A., Vasanthakumar A. (2018). Melding the old with the new: trends in methods used to identify, monitor, and control microorganisms on cultural heritage materials. Microb. Ecol. 76, 64–80. doi: 10.1007/s00248-016-0770-4, PMID: PubMed DOI

Segawa T., Matsuzaki R., Takeuchi N., Akiyoshi A., Navarro F., Sugiyama S., et al. . (2018). Bipolar dispersal of red-snow algae. Nat. Commun. 9:3094. doi: 10.1038/s41467-018-05521-w, PMID: PubMed DOI PMC

Smith H. D., Baqué M., Duncan A. G., Lloyd C. R., McKay C. P., Billi D. (2014). Comparative analysis of cyanobacteria inhabiting rocks with different light transmittance in the Mojave Desert: a Mars terrestrial analogue. Int. J. Astrobiol. 13, 271–277. doi: 10.1017/S1473550414000056 DOI

Sorrels C. M., Proteau P. J., Gerwick W. H. (2009). Organization, evolution, and expression analysis of the biosynthetic gene cluster for scytonemin, a cyanobacterial UV-absorbing pigment. Appl. Environ. Microbiol. 75, 4861–4869. doi: 10.1128/AEM.02508-08, PMID: PubMed DOI PMC

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

Stivaletta N., Lopez-Garcia P., Boihem L., Millie D. F., Barbieri R. (2010). Biomarkers of endolithic communities within gypsum crusts (southern Tunisia). Geomicrobiol. J. 27, 101–110. doi: 10.1080/01490450903410431 DOI

Storme J.-Y., Golubic S., Wilmotte A., Kleinteich J., Velázquez D., Javaux E. J. (2015). Raman characterization of the UV-protective pigment gloeocapsin and its role in the survival of cyanobacteria. Astrobiology 15, 843–857. doi: 10.1089/ast.2015.1292, PMID: PubMed DOI

Strunecký O., Ivanova A. P., Mareš J. (2022). An updated classification of cyanobacterial orders and families based on phylogenomic and polyphasic analysis. J. Phycol. 59, 12–51. doi: 10.1111/jpy.13304 PubMed DOI

Tang Y., Lian B., Dong H., Liu D., Hou W. (2012). Endolithic bacterial communities in dolomite and limestone rocks from the Nanjiang canyon in Guizhou karst area (China). Geomicrobiol. J. 29, 213–225. doi: 10.1080/01490451.2011.558560 PubMed DOI

Taton A., Grubisic S., Brambilla E., De Wit R., Wilmotte A. (2003). Cyanobacterial diversity in natural and artificial microbial mats of Lake Fryxell (McMurdo Dry Valleys, Antarctica): a morphological and molecular approach. Appl. Environ. Microbiol. 69, 5157–5169. doi: 10.1128/AEM.69.9.5157-5169.2003 PubMed DOI PMC

Villar S. E. J., Edwards H. G. M., Cockell C. S. (2005). Raman spectroscopy of endoliths from Antarctic cold desert environments. Analyst 130, 156–162. doi: 10.1039/b410854j, PMID: PubMed DOI

Vítek P., Ascaso C., Artieda O., Casero M. C., Wierzchos J. (2017). Discovery of carotenoid red-shift in endolithic cyanobacteria from the Atacama Desert. Sci. Rep. 7:11116. doi: 10.1038/s41598-017-11581-7, PMID: PubMed DOI PMC

Vítek P., Ascaso C., Artieda O., Casero M. C., Wierzchos J. (2020). Raman imaging of microbial colonization in rock—some analytical aspects. Anal. Bioanal. Chem. 412, 3717–3726. doi: 10.1007/s00216-020-02622-8, PMID: PubMed DOI

Vítek P., Jehlička J., Ascaso C., Mašek V., Gómez-Silva B., Olivares H., et al. . (2014b). Distribution of scytonemin in endolithic microbial communities from halite crusts in the hyperarid zone of the Atacama Desert, Chile. FEMS Microbiol. Ecol. 90, 351–366. doi: 10.1111/1574-6941.12387, PMID: PubMed DOI

Vítek P., Jehlička J., Edwards H. G. M., Hutchinson I., Ascaso C., Wierzchos J. (2012). The miniaturized Raman system and detection of traces of life in halite from the Atacama desert: some considerations for the search for life signatures on Mars. Astrobiology 12, 1095–1099. doi: 10.1089/ast.2012.0879, PMID: PubMed DOI PMC

Vítek P., Jehlicka J., Edwards H. G. M., Hutchinson I., Ascaso C., Wierzchos J. (2014a). Miniaturized Raman instrumentation detects carotenoids in Mars-analogue rocks from the Mojave and Atacama deserts. Philos. Trans. A Math. Phys. Eng. Sci. 372:20140196. doi: 10.1098/rsta.2014.0196, PMID: PubMed DOI

Walker J. J., Pace N. R. (2007). Endolithic microbial ecosystems. Annu. Rev. Microbiol. 61, 331–347. doi: 10.1146/annurev.micro.61.080706.093302 PubMed DOI

Wegley L., Edwards R., Rodriguez-Brito B., Liu H., Rohwer F. (2007). Metagenomic analysis of the microbial community associated with the coral Porites astreoides. Environ. Microbiol. 9, 2707–2719. doi: 10.1111/j.1462-2920.2007.01383.x, PMID: PubMed DOI

Whitton B. A. (2012). Ecology of cyanobacteria II: their diversity in space and time. Dorddrecht: Springer Science and Business Media.

Wierzchos J., Ascaso C., McKay C. P. (2006). Endolithic cyanobacteria in halite rocks from the hyperarid core of the Atacama Desert. Astrobiology 6, 415–422. doi: 10.1089/ast.2006.6.415, PMID: PubMed DOI

Wierzchos J., Casero M. C., Artieda O., Ascaso C. (2018). Endolithic microbial habitats as refuges for life in polyextreme environment of the Atacama Desert. Curr. Opin. Microbiol. 43, 124–131. doi: 10.1016/j.mib.2018.01.003, PMID: PubMed DOI

Wierzchos J., DiRuggiero J., Vítek P., Artieda O., Souza-Egipsy V., Škaloud P., et al. . (2015). Adaptation strategies of endolithic chlorophototrophs to survive the hyperarid and extreme solar radiation environment of the Atacama Desert. Front. Microbiol. 6:934. doi: 10.3389/fmicb.2015.00934, PMID: PubMed DOI PMC

Withnall R., Chowdhry B. Z., Silver J., Edwards H. G. M., de Oliveira L. F. (2003). Raman spectra of carotenoids in natural products. Spectrochim. Acta A Mol. Biomol. Spectrosc. 59, 2207–2212. doi: 10.1016/s1386-1425(03)00064-7, PMID: PubMed DOI

Wong F. K., Lau M. C., Lacap D. C., Aitchison J. C., Cowan D. A., Pointing S. B. (2010). Endolithic microbial colonization of limestone in a high-altitude arid environment. Microb. Ecol. 59, 689–699. doi: 10.1007/s00248-009-9607-8 PubMed DOI

Yung C. C., Chan Y., Lacap D. C., Pérez-Ortega S., de los Rios-Murillo A., Lee C. K., et al. . (2014). Characterization of chasmoendolithic community in miers valley, Mcmurdo dry valleys, Antarctica. Microb. Ecol. 68, 351–359. doi: 10.1007/s00248-014-0412-7 PubMed DOI

Zapomělová E., Hisem D., Řeháková K., Hrouzek P., Jezberová J., Komárková J., et al. . (2008). Experimental comparison of phenotypical plasticity and growth demands of two strains from the Anabaena circinalis/A. crassa complex (cyanobacteria). J. Plankton Res. 30, 1257–1269. doi: 10.1093/plankt/fbn081 DOI

Ziolkowski L., Mykytczuk N., Omelon C., Johnson H., Whyte L., Slater G. (2013). Arctic gypsum endoliths: a biogeochemical characterization of a viable and active microbial community. Biogeosciences 10, 7661–7675. doi: 10.5194/bg-10-7661-2013 DOI

Microbial colonization of gypsum: from the fossil record to the present day

Comparative analysis of cyanobacterial communities in gypsum outcrops: insights from sites in Israel and Poland

The underestimated fraction: diversity, challenges and novel insights into unicellular cyanobionts of lichens