ORIGINAL ARTICLE
 
KEYWORDS
ABSTRACT
Rocks are among the oldest terrestrial niches hosting a multiplicity of life forms, of which diversity has been only partially uncovered. Endolithic metacommunities comprise all major groups of microorganisms, such as chemo-organotrophic, chemo-lithotrophic and phototrophic, represented by bacteria, microalgae and microfungi. Their diversity is often difficult to describe and may remain underestimated. Furthermore, knowledge about the diversity of microorganisms colonizing rocks in peculiar niches is even poorer due to the difficulty to retrieve environmental specimens. Here, we report the phylogenetic and phenotypic characterization of a few endolithic fungi and algae isolated from rock fragments collected at high elevation, i.e., on the top of two mountains over 6000 m altitude, Muztagh Ata (China) and Cerro Mercendario (Argentina). The identity of the strains was confirmed by sequencing the nuclear ITS and LSU, the plastidial rbcL loci and by morphological analysis. Three fungal strains belonging to the class Dothideomycetes and one algal strain belonging to the genus Trebouxia were isolated from Muztagh Ata, while six fungal strains belonging to the order Chaetothyriales and four algal strains belonging to the genus Myrmecia were isolated from Cerro Mercedario. The detected species diversity is discussed in an evolutionary and ecological context.
FUNDING
This work was supported by the Italian Ministry of University and 12 Plant and Fungal Systematics 67(1): 1–16, 2022 Research (MIUR, Ministero dell’Università e della Ricerca) project PRIN2017 (project code 20177559A5) and by the University of Trieste microgrant funding program “D40_microgrants_ MUGGIA” assigned to LM.
 
REFERENCES (154)
1.
Ahmadjian, V. 1987. Coevolution in Lichens. Annals of the New York Academy of sciences 503: 307–315. https://doi.org/10.1111/j.1749....
 
2.
Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. 1990. Basic local alignment search tool. Journal of Molecular Biology 215: 403–410. https://doi.org/10.1016/S0022-....
 
3.
Alves, I. M. S., Gonçalves, V. N., Oliveira, F. S, Schaefer, C. E. G. R, Rosa, C. A. & Rosa, L. H. 2019. The diversity, distribution, and pathogenic potential of cultivable fungi present in rocks from the South Shetlands archipelago, Maritime Antarctica. Extremophiles 23: 327–336. https://doi.org/10.1007/s00792....
 
4.
Ametrano, C. G., Grewe, F., Crous, P. W., Goodwin, S. B., Liang, C., Selbmann, L., Lumbsch, T. H., Leavitt, S. D. & Muggia, L. 2019a. Genome-scale data resolve ancestral rock-inhabiting lifestyle in Dothideomycetes (Ascomycota). IMA Fungus 10: 1–12. https://doi.org/10.1186/s43008....
 
5.
Ametrano, C. G., Knudsen, K., Kocourková, J., Grube, M., Selbmann, L. & Muggia, L. 2019b. Phylogenetic relationships of rock-inhabiting black fungi belonging to the widespread genera Lichenothelia and Saxomyces. Mycologia 111: 127–160. https://doi.org/10.1080/002755....
 
6.
2018.1543510 Armstrong, R. A. 2017. Adaptation of lichens to extreme conditions. In: Shukla,V., Kumar, S. & Kumar, N., (eds) Plant adaptation strategies in changing environment, pp. 1–27. Springer, Singapore. https://doi.org/10.1007/978-98....
 
7.
Babič, M. N., Gunde-Cimerman, N., Vargha, M., Tischner, Z., Magyar, D., Veríssimo, C., Sabino, R., Viegas, C., Meyer, W. & Brandão, J. 2017. Fungal contaminants in drinking water regulation? A tale of ecology, exposure, purification and clinical relevance. International Journal of Environmental Research and Public Health 14: 636. https://doi.org/10.3390/ijerph....
 
8.
Baur, B., Fröberg, L. & Müller, S. W. 2007. Effect of rock climbing on the calcicolous lichen community of limestone cliffs in the northern Swiss Jura Mountains. Nova Hedwigia 85: 429–444. https://doi.org/10.1127/0029-5....
 
9.
Beck, A., Rambold, G. & Kasalicky, T. 2002. Myco-photobiontal selection in a Mediterranean cryptogam community with Fulgensia fulgida. New Phytologist 153: 317–326. https://doi.org/10.1046/j.0028....
 
10.
Bischoff, H. W. & Bold, H. C. 1963. Some soil algae from enchanted rock and related algae species. Phycological Studies 44: 1–95.
 
11.
Bjelland, T., Grube, M., Home, S., Jorgensen, S. L., Daae, F. L., Thorseth, I. H. & Øvreås, L. 2011. Microbial metacommunities in the lichen-rock habitat. Environmental Microbiology Reports 3: 434–442. https://doi.org/10.1111/j.1758....
 
12.
Bordenave, C. D., Muggia, L., Chiva, S., Leavitt, S. D., Carrasco, P. & Barreno, E. 2021. Chloroplast morphology and pyrenoid ultrastructural analyses reappraise the diversity of the lichen phycobiont genus Trebouxia (Chlorophyta). Algal Research 61: 102561. https://doi.org/10.1016/j.alga....
 
13.
Boustie, J., Tomasi, S. & Grube, M. 2011. Bioactive lichen metabolites: Alpine habitats as an untapped source. Phytochemistry Reviews 10: 287–307. https://doi.org/10.1007/s11101....
 
14.
Bruns, T. D. & Gardes, M. 1993. Molecular tools for the identification of ectomycorrhizal fungi-taxon‐specific oligonucleotide probes for suilloid fungi. Molecular Ecology 2: 233–242.
 
15.
Burford, E. P., Fomina, M. & Gadd, G. M. 2003. Fungal involvement in bioweathering and biotransformation of rocks and minerals. Mineralogical Magazine 67: 1127–1155. https://doi.org/10.1180/002646....
 
16.
Bubrick, P., Galun, M. & Frensdorff, A. 1984. Observation of free-living Trebouxia De Puymalyand Pseudotrebouxia Archibald, and evidence that boths symbionts from Xanthoria parietina (L.) Th. Fr. can be found free-living in nature. New Phytologist 97: 455–462. https://doi.org/10.1111/j.1469....
 
17.
Carter, N. E. A. & Viles, H. A. 2003. Experimental investigations into the interactions between moisture, rock surface temperatures and an epilithic lichen cover in the bioprotection of limestone. Building and Environment 38: 1225–1234. https://doi.org/10.1016/S0360-....
 
18.
Chomnunti, P., Bhat, D. J., Jones, E. B. G., Chukeatirote, E., Bahkali, A. H. & Hyde, K. D. 2012. Trichomeriaceae, a new sooty mould family of Chaetothyriales. Fungal Diversity 56: 63–76. https://doi.org/10.1007/s13225....
 
19.
Cockell, C., Rettberg, P., Horneck, G., Scherer, K. & Stokes, D. M. 2003. Measurements of microbial protection from ultraviolet radiation in polar terrestrial microhabitats. Polar Biology 26: 62–69. https://doi.org/10.1007/s00300....
 
20.
Coleine, C., Pombubpa, N., Zucconi, L., Onofri, S., Stajich, J. E. & Selbmann, L. 2020. Endolithic fungal species markers for harshest conditions in the McMurdo Dry Valleys, Antarctica. Life 10: 13. https://doi.org/10.3390/life10....
 
21.
Coleine, C., Stajich, J. E., de Los Ríos, A. & Selbmann, L. 2021. Beyond the extremes: Rocks as ultimate refuge for fungi in drylands. Mycologia 113: 108–133.
 
22.
Coleine, C., Delgado-Baquerizo, M., Albanese, D., Singh, B. K., Stajich, J. E., Selbmann, L. & Egidi, E. 2022. Rocks support a distinctive and consistent mycobiome across contrasting dry regions of Earth. FEMS Microbiology Ecology 98. https://doi.org/10.1093/femsec....
 
23.
Crits-Christoph, A., Gelsinger, D. R., Ma, B., Wierzchos, J., Ravel, J., Davila, A., Casero, M. C. & DiRuggiero, J. 2016. Functional interactions of archaea, bacteria and viruses in a hypersaline endolithic community. Environmental Microbiology 18: 2064–2077. https://doi.org/10.1111/1462-2....
 
24.
Cubero, O. F., Crespo, A., Fatehi, J. & Bridge, P. D. 1999. DNA extraction and PCR amplification method suitable for fresh, herbarium- stored, lichenized, and other fungi. Plant Systematics and Evolution 216: 243–249. https://doi.org/10.1007/BF0108....
 
25.
Cutler, N. A., Chaput, D. L., Oliver, A. E. & Viles, H. A. 2015. The spatial organization and microbial community structure of an epilithic biofilm. FEMS Microbiology Ecology 91. https://doi.org/10.1093/femsec....
 
26.
Dadachova, E. & Casadevall, A. 2008. Ionizing radiation: how fungi cope, adapt, and exploit with the help of melanin. Current Opinion in Microbiology 11: 525–531.
 
27.
De Carolis, R., Cometto, A., Moya, P., Barreno, E., Grube, M., Tretiach, M., Leavitt, S. D. & Muggia, L. 2022. Photobiont diversity in lichen symbioses from extreme environments. Frontiers in Microbiology 13: 809804. https://doi.org/10.3389/fmicb.....
 
28.
De Hoog, G. S., Guarro, J., Gené, J., Ahmed, S., Al-Hatmi, A. M. S., Figueras, M. J. & Vitale, R. G. 2019. Atlas of Clinical Fungi, 3rd e-edition. Utrecht/Reus.
 
29.
De Hoog, G. S. 2014. Ecology and phylogeny of black yeast-like fungi: diversity in unexplored habitats. Fungal Diversity 65: 1–2. https://doi.org/10.1007/s13225....
 
30.
De Jong, R., Von Gunten, L., Maldonado, A. & Grosjean, M. 2013. Late Holocene summer temperatures in the central Andes reconstructed from the sediments of high-elevation Laguna Chepical, Chile (32 S). Climate of the Past 9: 19211–1932. https://doi.org/10.5194/cp-9-1....
 
31.
De la Torre, J. R., Goebel, B. M., Friedmann, E. I. & Pace, N. R. 2003. Microbial diversity of cryptoendolithic communities from the McMurdo Dry Valleys, Antarctica. Applied and Environmental Microbiology 69: 3858–3867. https://doi.org/10.1128/AEM.69....
 
32.
De Los Ríos, A., Grube, M., Sancho, L. G. & Ascaso, C. 2007. Ultrastructural and genetic characteristics of endolithic cyanobacterial biofilms colonizing Antarctic granite rocks. FEMS Microbiology Ecology 59: 386–395. https://doi.org/10.1111/j.1574....
 
33.
De Los Ríos, A., Wierzchos, J. & Ascaso, C. 2014. The lithic microbial ecosystems of Antarctica’s McMurdo Dry Valleys. Antarctic Science 25: 459–477. https://doi.org/10.1017/S09541....
 
34.
De Los Ríos, A., Wierzchos, J., Sancho, L. G., Green, T. A. & Ascaso, C. 2005. Ecology of endolithic lichens colonizing granite in continental Antarctica. The Lichenologist 37: 383–395. https://doi.org/10.1017/S00242....
 
35.
De Menezes, G. C. A., Câmara, P. E. A. S., Pinto, O. H. B., Carvalho- Silva, M., Oliveira, F. S., Souza, C. D., Reynaud Schaefer C. E. G., Convey, P., Rosa, C. A. & Rosa, L. H. 2021. Fungal diversity present on rocks from a polar desert in continental Antarctica assessed using DNA metabarcoding. Extremophiles 25: 193–202. https://doi.org/10.1007/s00792....
 
36.
Diels, L. 1914. Die Algen-Vegetation der Südtiroler Dolomitriffe: Ein Beitrag zur Ökologie der Lithophyten. Borntraeger.
 
37.
DiRuggiero, J., Wierzchos, J., Robinson, C. K., Souterre, T., Ravel, J., Artieda, O., Souza-Egipsy, V. & Ascaso, C. 2013. Microbial colonisation of chasmoendolithic habitats in the hyper-arid zone of the Atacama Desert. Biogeosciences 10: 2439–2450. https://doi.org/10.5194/bg-10-....
 
38.
Egidi, E., De Hoog, G. S., Isola, D., Onofri, S., Quaedvlieg, W., De Vries, M., Verkley, G. J. M., Stielow, J. B., Zucconi, L. & Selbmann, L. 2014. Phylogeny and taxonomy of meristematic rock-inhabiting black fungi in the Dothideomycetes based on multi-locus phylogenies. Fungal Diversity 65: 127–165. https://doi.org/10.1007/s13225....
 
39.
Farrell, R. L., Arenz, B. E., Duncan, S. M., Held, B. W., Jurgens, J. A. & Blanchette, R. A. 2011. Introduced and indigenous fungi of the Ross Island historic huts and pristine areas of Antarctica. Polar Biology 34: 1669–1677. https://doi.org/10.1007/s00300....
 
40.
Flechtner, V. R., Pietrasiak, N. & Lewis, L. A. 2013. Newly revealed diversity of green microalgae from wilderness areas of Joshua Tree National Park (JTNP). Monographs of the Western North American Naturalist 6: 43–63. https://doi.org/10.3398/042.00....
 
41.
Frenot, Y., Chown, S. L., Whinam, J., Selkirk, P. M., Convey, P., Skotnicki, M. & Bergstrom, D. M. 2005. Biological invasions in the Antarctic: extent, impacts and implications. Biological Reviews of the Cambridge Philosophical Society 80: 45–72. https://doi.org/10.1017/S14647....
 
42.
Friedmann, E. I. 1982. Endolithic microorganisms in the Antarctic cold desert. Science 215: 1045–1053. https://doi.org/10.1126/scienc....
 
43.
Friedmann, E. I. & Galun, M. 1974. Desert biology. Academic Press, New York.
 
44.
Friedmann, E. I. & Ocampo-Friedmann, R. 1984. The antarctic cryptoendolithic ecosystem: relevance to exobiology. Origins of Life 14: 771–776. https://doi.org/10.1007/BF0093....
 
45.
Fučíková, K., Lewis, P. O. & Lewis, L. A. 2014. Widespread desert affiliation of trebouxiophycean algae (Trebouxiophyceae, Chlorophyta) including discovery of three new desert genera. Phycological Research 62: 294–305. https://doi.org/10.1111/pre.12....
 
46.
Gadd, G. M. 2007. Geomycology: biogeochemical transformations of rocks, minerals, metals and radionuclides by fungi, bioweathering and bioremediation. Mycological Research 111: 3–49.
 
47.
Gaylarde, P., Englert, G., Ortega-Morales, O. & Gaylarde, C. 2006. Lichen-like colonies of pure Trentepohlia on limestone monuments. International Biodeterioration and Biodegradation 58: 119–123. https://doi.org/10.1016/j.ibio....
 
48.
Golubic, S., Friedmann, I. & Schneider, J. 1981. The lithobiontic ecological niche, with special reference to microorganisms. Journal of Sedimentary Petrology 51: 475– 478. https://doi.org/10.1306/212F-7....
 
49.
Gómez-Alarcón, G., Muñoz, M., Ariño, X. & Ortega-Calvo, J. J. 1995. Microbial communities in weathered sandstones: the case of Carrascosa del Campo church, Spain. Science of the Total Environment 167: 249–254. https://doi.org/10.1016/0048-9....
 
50.
Gómez-Silva, B. 2018. Lithobiontic life: “Atacama rocks are well and alive.” Antonie van Leeuwenhoek, International Journal of General and Molecular Microbiology 111: 1333–1343. https://doi.org/10.1007/s10482....
 
51.
Gorbushina, A. A. 2007. Life on the rocks. Environmental Microbiology 9: 1613–1631.
 
52.
Gorbushina, A. A., Beck, A. & Schulte, A. 2005. Microcolonial rock inhabiting fungi and lichen photobionts: evidence for mutualistic interactions. Mycological Research 109: 1288–1296. https://doi.org/10.1017/S09537....
 
53.
Gorbushina, A. A., Kotlova, E. R. & Sherstneva, O. A. 2008. Cellular responses of microcolonial rock fungi to long-term desiccation and subsequent rehydration. Studies in Mycology 61: 91–97. https://doi.org/10.3114/sim.20....
 
54.
Gorbushina, A. A. & Petersen, K. 2000. Distribution of microorganisms on ancient wall paintings as related to associated faunal elements. International Biodeterioration and Biodegradation 46: 277–284. https://doi.org/10.1016/S0964-....
 
55.
Gostinčar, C. 2020. Towards genomic criteria for delineating fungal species. Journal of Fungi 6: 246. https://doi.org/10.3390/jof604....
 
56.
Gostinčar, C., Gunde-Cimerman, N. & Turk, M. 2012a. Genetic resources of extremotolerant fungi: a method for identification of genes conferring stress tolerance. Bioresource Technology 111: 246. https://doi.org/10.1016/j.bior....
 
57.
Gostinčar, C., Lenassi, M., Gunde-Cimerman, N. & Plemenitaš, A. 2011. Fungal adaptation to extremely high salt concentrations. In Advances in applied microbiology 77: 71–96. https://doi.org/10.1016/B978-0....
 
58.
Gostinčar, C., Muggia, L. & Grube, M. 2012b. Polyextremotolerant black fungi: oligotrophism, adaptive potential, and a link to lichen symbioses. Frontiers in Microbiology 3: 390. https://doi.org/10.3389/fmicb.....
 
59.
Gueidan, C., Ruibal, C., De Hoog, G. S. & Schneider, H. 2011. Rock-inhabiting fungi originated during periods of dry climate in the late Devonian and middle Triassic. Fungal Biology 115: 987–996. https://doi.org/10.1016/j.funb....
 
60.
Gueidan, C., Villaseñor, C. R., De Hoog, G. S., Gorbushina, A. A., Untereiner, W. A. & Lutzoni, F. 2008. A rock-inhabiting ancestor for mutualistic and pathogen-rich fungal lineages. Studies in Mycology 61: 111–119. https://doi.org/10.3114/sim.20....
 
61.
Gunde-Cimerman. N., Grube, M. & De Hoog, G. S. 2011. The emerging potential of melanized fungi: black yeast between beauty and the beast. Fungal Biology 115: 935–936.
 
62.
Hall, T. A. 1999. BIOEDIT: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/ NT. Nucleic Acids Symposium Series 41.
 
63.
Hartmann, M., Lee, S., Hallam, S. J. & Mohn, W. W. 2009. Bacterial, archaeal and eukaryal community structures throughout soil horizons of harvested and naturally disturbed forest stands. Environmental Microbiology 11: 3045–3062. https://doi.org/10.1111/j.1462....
 
64.
Harutyunyan, S., Muggia, L. & Grube, M. 2008. Black fungi in lichens from seasonally arid habitats. Studies in Mycology 61: 83–90. https://doi.org/10.3114/sim.20....
 
65.
Hirsch, P., Eckhardt, F. E. W. & Palmer, R. J. 1995. Methods for the study of rock-inhabiting microorganisms-A mini review. Journal of Microbiological Methods 23: 143–167.
 
66.
Hoffmann, L. 1989. Algae of terrestrial habitats. The Botanical Review 55: 77–105. https://doi.org/10.1007/BF0285....
 
67.
Isola, D., Zucconi, L., Onofri, S., Caneva, G., De Hoog, G. S. & Selbmann, L. 2016. Extremotolerant rock inhabiting black fungi from Italian monumental sites. Fungal Diversity 76: 75–96. https://doi.org/10.1007/s13225....
 
68.
Jackson, T. A. 2015. Weathering, secondary mineral genesis, and soil formation caused by lichens and mosses growing on granitic gneiss in a boreal forest environment. Geoderma 251: 79–91. https://doi.org/10.1016/j.geod....
 
69.
James, T. Y., Stajich, J. E., Hittinger, C. T. & Rokas, A. 2020. Toward a fully resolved fungal tree of life. Annual Review of Microbiology 74: 291–313.
 
70.
Katoh, K. & Standley, D. M. 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30: 772–780. https://doi.org/10.1093/molbev....
 
71.
Khan, A., Kong, W., Ji, M., Yue, L., Xie, Y., Liu, J. & Xu, B. 2020. Disparity in soil bacterial community succession along a short timescale deglaciation chronosequence on the Tibetan Plateau. Soil Ecology Letters 2: 83–92. https://doi.org/10.1007/s42832....
 
72.
Kinnard, C., Ginot, P., Surazakov, A., MacDonell, S., Nicholson, L., Patris, N., Rabatel, A., Rivera, A. & Squeo, F. A. 2020. Mass balance and climate history of a high-altitude glacier, Desert Andes of Chile. Frontiers in Earth Science 8: 40. https://doi.org/10.3389/feart.....
 
73.
Kogej, T., Ramos, J., Plemenitaš, A. & Gunde-Cimerman, N. 2005. The halophilic fungus Hortaea werneckii and the halotolerant fungus Aureobasidium pullulans maintain low intracellular cation concentrations in hypersaline environments. Applied and Environmental Microbiology 71: 6600–6605. https://doi.org/10.1128/AEM.71....
 
74.
Kroken, S. & Taylor, J. W. 2000. Phylogenetic species, reproductive mode, and specificity of the green alga Trebouxia forming lichens with the fungal genus Letharia. Bryologist 103: 645–660. https://doi.org/10.1639/0007-2....
 
75.
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: 1547–1549. https://doi.org/10.1093/molbev....
 
76.
Kumar, S., Suyal, D. C., Yadav, A., Shouche, Y. & Goel, R. 2019. Microbial diversity and soil physiochemical characteristic of higher altitude. PLoS ONE 14: e0213844. https://doi.org/10.1371/journa....
 
77.
Leavitt, S. D., Kraichak, E., Nelsen, M. P., Altermann, S., Divakar, P. K., Alors, D., Esslinger, T. L., Crespo, A. & Lumbsch, T. 2015. Fungal specificity and selectivity for algae play a major role in determining lichen partnerships across diverse ecogeographic regions in the lichen‐forming family Parmeliaceae (Ascomycota). Molecular Ecology 24: 3779–3797.
 
78.
Letunic, I. & Bork, P. 2019. Interactive Tree of Life (iTOL) v4: Recent updates and new developments. Nucleic Acids Research 47: 256–259. https://doi.org/10.1093/nar/gk....
 
79.
Lewis, L. A. & Lewis, P. O. 2005. Unearthing the molecular phylodiversity of desert soil green algae (Chlorophyta). Systematic Biology 54: 936–947. https://doi.org/10.1080/106351....
 
80.
Liu, Y., He, J., Shi, G., An, L., Öpik, M. & Feng, H. 2011. Diverse communities of arbuscular mycorrhizal fungi inhabit sites with very high altitude in Tibet Plateau. FEMS Microbiology Ecology 78: 355–365. https://doi.org/10.1111/j.1574....
 
81.
Matthes, U., Turner, S. J. & Larson, D. W. 2001. Light attenuation by limestone rock and its constraint on the depth distribution of endolithic algae and cyanobacteria. International Journal of Plant Sciences 162: 263–270. https://doi.org/10.1086/319570.
 
82.
Miller, M. A., Pfeiffer, W. & Schwartz, T. 2011. The CIPRES science gateway: A community resource for phylogenetic analyses. In: Proceedings of the TeraGrid 2011 Conference: Extreme Digital Discovery, pp. 1–8.
 
83.
Moya, P., Chiva, S., Molins, A., Jadrná, I., Škaloud, P., Peksa, O. & Barreno, E. 2018. Myrmecia israeliensis as the primary symbiotic microalga in squamulose lichens growing in European and Canary Island terricolous communities. Fottea 18: 72–85. https://doi.org/10.5507/fot.20....
 
84.
Muggia, L., Fleischhacker, A., Kopun, T. & Grube, M. 2016. Extremotolerant fungi from alpine rock lichens and their phylogenetic relationships. Fungal Diversity 76: 119–142. https://doi.org/10.1007/s13225....
 
85.
Muggia, L., Nelsen, M. P., Kirika, P. M., Barreno, E., Beck, A., Lindgren, H., Lumbsch, T. H., Leavitt, S. D. & Trebouxia working group 2020. Formally described species woefully underrepresent phylogenetic diversity in the common lichen photobiont genus Trebouxia (Trebouxiophyceae, Chlorophyta): An impetus for developing an integrated taxonomy. Molecular Phylogenetics and Evolution 149. https://doi.org/10.1016/j.ympe....
 
86.
Muggia, L., Quan, Y., Gueidan, C., Al-Hatmi, A., Grube, M. & de Hoog, S. 2021. Sequence data from isolated lichen-associated melanized fungi enhance delimitation of two new lineages within Chaetothyriomycetidae. Mycological Progress 20: 911–927. https://doi.org/10.1007/s11557....
 
87.
Mutawalli, L., Syaifur Rizal, M. R., Artama, W. T., Fajriyah, R., Muhimmah, I. & Rujito, L. 2019. Analisa visual menggunakan etetoolkit framework terhadap penyakit beta-thalassemia di jawa tengah begian selatan. Jurnal Informatika dan Rekayasa Elektronik 2: 16–27. https://doi.org/10.36595/jire.....
 
88.
Nelsen, M. P., Plata, E. R., Andrew, C. J., Lücking, R. & Lumbsch, H. T. 2011. Phylogenetic diversity of trentepohlialean algae associated with lichen-forming fungi. Journal of Phycology 47: 282–290. https://doi.org/10.1111/j.1529....
 
89.
Nelson, D. R., Bartels, P. J. & Fegley, S. R. 2020. Environmental correlates of tardigrade community structure in mosses and lichens in the Great Smoky Mountains National Park (Tennessee and North Carolina, USA). Zoological Journal of the Linnean Society 188: 913–924. https://doi.org/10.1093/zoolin....
 
90.
Nienow, J. A., McKay, C. P. & Friedmann, E. I. 1988. The cryptoendolithic microbial environment in the Ross Desert of Antarctica: mathematical models of the thermal regime. Microbial Ecology 16: 253–270. https://doi.org/10.1007/BF0201....
 
91.
Ogwu, M. C., Takahashi, K., Dong K, Song, H. K., Moroenyane, I., Waldman, B. & Adams, J. M. 2019. Fungal elevational rapoport pattern from a high mountain in Japan. Scientific Reports 9: 1–10. https://doi.org/10.1038/s41598....
 
92.
Olech, M. & Chwedorzewska, K. J. 2011. Short Note: the first appearance and establishment of an alien vascular plant in natural habitats on the forefield of a retreating glacier in Antarctica. Antarctic Science 23: 153–154.
 
93.
Omelon, C. R. 2008. Endolithic microbial communities in polar desert habitats. Geomicrobiology Journal 25: 404–414. https://doi.org/10.1080/014904....
 
94.
Onofri, S., Selbmann, L., De Hoog, G. S., Grube, M., Barreca, D., Ruisi, S. & Zucconi, L. 2007b. Evolution and adaptation of fungi at boundaries of life. Advances in Space Research 40: 1657–1664. https://doi.org/10.1016/j.asr.....
 
95.
Onofri, S., Zucconi, L., Isola, D. & Selbmann, L. 2014. Rock-inhabiting fungi and their role in deterioration of stone monuments in the Mediterranean area. Plant Biosystems – An International Journal Dealing with all Aspects of Plant Biology 148: 384–391. https://doi.org/10.1080/112635....
 
96.
Onofri, S., Zucconi, L., Selbmann, L., Hoog, S. D., Ríos, D. A. D. L., Ruisi, S. & Grube, M. 2007a. Fungal Associations at the Cold Edge of Life. In: Seckbach, J. (eds) Algae and Cyanobacteria in Extreme Environments. Cellular Origin, Life in Extreme Habitats and Astrobiology, vol 11. Springer, Dordrecht, pp. 735–757. https://doi.org/10.1007/978-1-....
 
97.
Ortega-Morales, O., Guezennec, J., Hernandez-Duque, G., Gaylarde, C. C. & Gaylarde, P. M. 2000. Phototrophic biofilms on ancient Mayan buildings in Yucatan, Mexico. Current Microbiology 40: 81–85. https://doi.org/10.1007/s00284....
 
98.
Pacelli, C., Cassaro, A., Maturilli, A., Timperio, A. M., Gevi, F., Cavalazzi, B., Stefan, M., Ghica, D. & Onofri, S. 2020. Multidisciplinary characterization of melanin pigments from the black fungus Cryomyces antarcticus. Applied Microbiology and Biotechnology 104: 6385–6395. https://doi.org/10.1007/s00253....
 
99.
Peel, M. C., Finlayson, B. L. & McMahon, T. A. 2007. Updated world map of the Köppen-Geiger climate classification. Hydrology and Earth System Sciences 11: 1633–1644. https://doi.org/10.5194/hess-1....
 
100.
Peraza Zurita, Y., Cultrone, G., Sánchez Castillo P., Sebastián, E. & Bolívar, F. C. 2005. Microalgae associated with deteriorated stonework of the fountain of Bibatauín in Granada, Spain. International Biodeterioration & Biodegradation 55: 55–61. https://doi.org/10.1016/j.ibio....
 
101.
Piñar, G., Dalnodar, D., Voitl, C., Reschreiter, H. & Sterflinger, K. 2016. Biodeterioration risk threatens the 3100 year old staircase of hallstatt (Austria): possible involvement of halophilic microorganisms. PLoS ONE 11. https://doi.org/10.1371/journa....
 
102.
Pitkäranta, M., Meklin, T., Hyvärinen, A., Nevalainen, A., Paulin, L., Auvinen, P., Lignell, U. & Rintala, H. 2011. Molecular profiling of fungal communities in moisture damaged buildings before and after remediation-a comparison of culture-dependent and culture- independent methods. BMC Microbiology 11: 1–16. https://doi.org/10.1186/1471-2....
 
103.
Pointing, S. B., Chan, Y., Lacap, D. C., Lau, M. C., Jurgens, J. A. & Farrell, R. L. 2009. Highly specialized microbial diversity in hyper-arid polar desert. Proceedings of the National Academy of Sciences 106: 19964–19969. https://doi.org/10.1073/pnas.0....
 
104.
Praeg, N., Seeber, J., Leitinger, G., Tasser, E., Newesely, C., Tappeiner, U. & Illmer, P. 2020. The role of land management and elevation in shaping soil microbial communities: insights from the Central European Alps. Soil Biology and Biochemistry 150: 107951. https://doi.org/10.1016/j.soil....
 
105.
Quan, Y., Muggia, L., Moreno, L. F., Wang, M., Al-Hatmi, A., da Silva Menezes, N., Shi, D., Deng, S., Ahmed, S., Hyde, K. D., Vicente, V. A., Kang, Y., Stielow, J. B. & de Hoog, S. 2020. A re-evaluation of the Chaetothyriales using criteria of comparative biology. Fungal Diversity 103: 47–85. https://doi.org/10.1007/s13225....
 
106.
R Development Core Team (2019) R Core Team (2020). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/.
 
107.
R Foundation for Statistical Computing 2 Rambold, G., Friedl, T. & Beck, A. 1998. Photobionts in Lichens: possible indicators of phylogenetic relationships? Bryologist 101: 392–397. https://doi.org/10.1639/0007-2....
 
108.
Robinson, C. K., Wierzchos, J., Black, C., Crits‐Christoph, A., Ma, B., Ravel, J., Ascaso, A., Artieda, O., Valea, S., Roldán, M., Gómez- Silva, B. & DiRuggiero, J. 2015. Microbial diversity and the presence of algae in halite endolithic communities are correlated to atmospheric moisture in the hyper‐arid zone of the Atacama Desert. Environmental microbiology 17: 299–315. https://doi.org/10.1111/1462-2....
 
109.
Robinson, D. F. & Foulds, L. R. 1981. Comparison of phylogenetic trees. Mathematical Biosciences 53: 131–147. https://doi.org/10.1016/0025-5....
 
110.
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: 539–542. https://doi.org/10.1093/sysbio....
 
111.
Ruibal, C., Gueidan, C., Selbmann, L., Gorbushina, A. A., Crous, P. W., Groenewald, J. Z., Muggia, L., Grube, M., Isola, D., Schoch, C. L., Staley, J. T., Lutzoni, F. & De Hoog, G. S. 2009. Phylogeny of rock-inhabiting fungi related to Dothideomycetes. Studies in Mycology 64: 131–136. https://doi.org/10.3114/sim.20....
 
112.
Ruibal, C., Platas, G. & Bills, G. F. 2005. Isolation and characterization of melanized fungi from limestone formations in Mallorca. Mycological Progress 4: 23–38. https://doi.org/10.1007/s11557....
 
113.
Samolov, E., Baumann, K., Büdel, B., Jung, P., Leinweber, P., Mikhailyuk, T., Karsten, U. & Glaser, K. 2020. Biodiversity of algae and cyanobacteria in biological soil crusts collected along a climatic gradient in Chile using an integrative approach. Microorganisms 8: 1047. https://doi.org/10.3390/microo....
 
114.
Samsonoff, W. A. & MacColl, R. 2001. Biliproteins and phycobilisomes from cyanobacteria and red algae at the extremes of habitat. Archives of Microbiology 176: 400–405.
 
115.
Selbmann, L., Grube, M., Onofri, S., Isola, D. & Zucconi, L. 2013. Antarctic epilithic lichens as niches for black meristematic fungi. Biology 2: 784–797. https://doi.org/10.3390/biolog....
 
116.
Selbmann, L., Isola, D., Egidi, E., Zucconi, L., Gueidan, C., De Hoog, G. S. & Onofri, S. 2014. Mountain tips as reservoirs for new rock-fungal entities: Saxomyces gen. nov. and four new species from the Alps. Fungal Diversity 65: 167–182. https://doi.org/10.1007/s13225....
 
117.
Selbmann, L., Isola, D., Zucconi, L. & Onofri, S. 2011. Resistance to UV-B induced DNA damage in extreme-tolerant cryptoendolithic Antarctic fungi: detection by PCR assays. Fungal Biology 115: 937–944. https://doi.org/10.1016/j.funb....
 
118.
Selbmann, L., Onofri, S., Coleine, C., Buzzini, P., Canini, F. & Zucconi, L. 2017. Effect of environmental parameters on biodiversity of the fungal component in lithic Antarctic communities. Extremophiles 21: 1069–1080. https://doi.org/10.1007/s00792....
 
119.
Selbmann, L., Stoppiello, G. A., Onofri, S., Stajich, J. E. & Coleine, C. 2021. Culture-dependent and amplicon sequencing approaches reveal diversity and distribution of black fungi in Antarctic cryptoendolithic communities. Journal of Fungi 7: 213. https://doi.org/10.3390/jof703....
 
120.
Selbmann, L., Zucconi, L., Isola, D. & Onofri, S. 2015. Rock black fungi: excellence in the extremes, from the Antarctic to space. Current Genetics 61: 335–345. https://doi.org/10.1007/s00294....
 
121.
Seong, Y. B., Owen, L. A., Yi, C. & Finkel, R. C. 2009. Quaternary glaciation of Muztag Ata and Kongur Shan: evidence for glacier response to rapid climate changes throughout the late glacial and holocene in westernmost Tibet. Bulletin of the Geological Society of America 121: 346–365. https://doi.org/10.1130/B26339....
 
122.
Shangguan, D., Liu, S., Ding, Y., Ding, L., Xiong, L., Cai, D., Li, G., Lu, A., Zhang, S. & Zhang, Y. 2006. Monitoring the glacier changes in the Muztag Ata and Konggur mountains, east Pamirs, based on Chinese Glacier Inventory and recent satellite imagery. Annals of Glaciology 43: 79–85.
 
123.
Souza‐Egipsy, V., Wierzchos, J., Sancho, C., Belmonte, A. & Ascaso, C. 2004. Role of biological soil crust cover in bioweathering and protection of sandstones in a semi‐arid landscape (Torrollones de Gabarda, Huesca, Spain). Earth Surface Processes and Landforms: The Journal of the British Geomorphological Research Group 29: 1651–1661. https://doi.org/10.1002/esp.11....
 
124.
Spitale, D. & Nascimbene, J. 2012. Spatial structure, rock type, and local environmental conditions drive moss and lichen distribution on calcareous boulders. Ecological Research 27: 633–638. https://doi.org/10.1007/s11284....
 
125.
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/bioinf....
 
126.
Sterflinger, K. 1998. Temperature and NaCl- tolerance of rock-inhabiting meristematic fungi. Antonie van Leeuwenhoek, International Journal of General and Molecular Microbiology 74: 271–281. https://doi.org/10.1023/A:1001....
 
127.
Stevens, G. C. 1992. The elevational gradient in altitudinal range: an extension of Rapoport’s latitudinal rule to altitude. American Naturalist 140: 893–911. https://doi.org/10.1086/285447.
 
128.
Stevens, G. C. 1989. The latitudinal gradient in geographical range: how so many species coexist in the tropics. American Naturalist 133: 240–256. https://doi.org/10.1086/284913.
 
129.
Su, L., Guo, L., Hao, Y., Xiang, M., Cai, L. & Liu, X. 2015. Rupestriomyces and Spissiomyces, two new genera of rock-inhabiting fungi from China. Mycologia 107: 831–844. https://doi.org/10.3852/14-305.
 
130.
Tanaka, D., Sato, K., Goto, M., Fujiyoshi, S., Maruyama, F., Takato, S., Shimada, T., Sakatoku, A., Aoki, K. & Nakamura, S. 2019. Airborne microbial communities at high-altitude and suburban sites in Toyama, Japan suggest a new perspective for bioprospecting. Frontiers in Bioengineering and Biotechnology 7: 12.
 
131.
Tang, M., Li, L., Wang, X., You, J., Li, J. & Chen, X. 2020. Elevational is the main factor controlling the soil microbial community structure in alpine tundra of the Changbai Mountain. Scientific Reports 10: 1–15. https://doi.org/10.1038/s41598....
 
132.
Teixeira, M. D. M., Moreno, L. F., Stielow, B. J., Muszewska, A., Hainaut, M., Gonzaga, L., Abouelleil, A., Patané, J. S. L., Priest, M., Souza, R., Young, S., Ferreira, K. S., Zeng, Q. Da Cunha, M. M. L., Gladki, A., Barker, B., Vicente, V. A., De Souza, E. M., Almeida, S., Henrissat, B., Vasconcelos, A. T. R., Deng, S., Voglmayr, H., Moussa, T. A. A., Gorbushina, A., Felipe, A., Cuomo, C. A. & de Hoog, G. S. 2017. Exploring the genomic diversity of black yeasts and relatives (Chaetothyriales, Ascomycota). Studies in Mycology 86: 1–28. https://doi.org/10.1016/j.simy....
 
133.
Tschermak-Woess, E. 2019. The Algal Partner. In Handbook of Lichenology. https://doi.org/10.1201/978042....
 
134.
Velázquez, M. S., Stürmer, S. L., Bruzone, C., Fontenla, S., Barrera, M. & Cabello, M. 2016. Occurrence of arbuscular mycorrhizal fungi in high altitude sites of the Patagonian Altoandina Region in Nahuel Huapi National Park (Argentina). Acta Botanica Brasilica 30. https://doi.org/10.1590/0102-3....
 
135.
Vilgalys, R. & Hester, M. 1990. Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. Journal of Bacteriology 172: 4238–4246. https://doi.org/10.1128/jb.172....
 
136.
Vincent, W. F. 1988. Microbial ecosystems of Antarctica. Cambridge University Press. https://doi.org/10.2307/155130....
 
137.
Walker, J. J. & Pace, N. R. 2007. Phylogenetic composition of rocky mountain endolithic microbial ecosystems. Applied and Environmental Microbiology 73: 3497–3504. https://doi.org/10.1128/AEM.02....
 
138.
Wei, S. T., Lacap-Bugler, D. C., Lau, M. C., Caruso, T., Rao, S., De Los Rios, A., Archer, S. K., Chiu, J. M. Y., Higgins, C., Van Nostrand, J. D., Zhou, J., Hopkins, D. W. & Pointing, S. B. 2016. Taxonomic and functional diversity of soil and hypolithic microbial communities in Miers Valley, McMurdo Dry Valleys, Antarctica. Frontiers in Microbiology 7: 1642. https://doi.org/10.3389/fmicb.....
 
139.
White, T. J., Bruns, T., Lee, S. & Taylor, J. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR protocols: a guide to methods and applications 8: 315–322.
 
140.
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. https://doi.org/10.1089/ast.20....
 
141.
Wierzchos, J., Cámara, B., de Los Ríos, A., Davila, A. F., Sánchez Almazo, I. M., Artieda, O., Wierzchos, K., Gómez-Silva, B., McKay, C. & Ascaso, C. 2011. Microbial colonization of Ca-sulfate crusts in the hyperarid core of the Atacama Desert: implications for the search for life on Mars. Geobiology 9: 44–60. https://doi.org/10.1111/j.1472....
 
142.
Wierzchos, J., de Los Ríos, A. & Ascaso, C. 2012. Microorganisms in desert rocks: the edge of life on Earth. International Microbiology 15: 171–181. https://doi.org/10.2436/20.150....
 
143.
Wierzchos, J., DiRuggiero, J., Vítek, P., Artieda, O., Souza-Egipsy, V., Skaloud, P., Tisza, M., Davila, A., Vílchez, C., Garbayo, I. & Ascaso, C. 2015. Adaptation strategies of endolithic chlorophototrophs to survive the hyperarid and extreme solar radiation environment of the Atacama Desert. Frontiers in Microbiology 6: 934. https://doi.org/10.3389/fmicb.....
 
144.
Wijayawardene, N. N., Bahram, M., Sánchez-Castro, I., Dai, D. Q., Ariyawansa, K. G., Jayalal, U., Suwannarach, N. & Tedersoo, L. 2021. Current insight into culture-dependent and culture-independent methods in discovering Ascomycetous Taxa. Journal of Fungi 7: 703. https://doi.org/10.3390/jof709....
 
145.
Wollenzien, U., De Hoog, G. S., Krumbein, W. E. & Urzí, C. 1995. On the isolation of microcolonial fungi occurring on and in marble and other calcareous rocks. Science of the Total Environment 167: 287–294. https://doi.org/10.1016/0048-9....
 
146.
Wong, F. K., Lacap, D. C., Lau, M. C., Aitchison, J. C., Cowan, D. A. & Pointing, S. B. 2010. Hypolithic microbial community of quartz pavement in the high-altitude tundra of central Tibet. Microbial Ecology 60: 730–739. https://doi.org/10.1007/s00248....
 
147.
Xiang, S., Yao, T., An, L., Xu, B. & Wang, J. 2005. 16S rRNA sequences and differences in bacteria isolated from the Muztag Ata glacier at increasing depths. Applied and Environmental Microbiology 71: 4619–4627. https://doi.org/10.1128/AEM.71....
 
148.
Yamamoto, N., Bibby, K., Qian, J., Hospodsky, D., Rismani-Yazdi, H., Nazaroff, W. W. & Peccia, J. 2012. Particle-size distributions and seasonal diversity of allergenic and pathogenic fungi in outdoor air. The ISME Journal 6: 1801–1811. https://doi.org/10.1038/ismej.....
 
149.
Yan, S., Guo, H., Liu, G. & Ruan, Z. 2013. Mountain glacier displacement estimation using a DEM-assisted offset tracking method with ALOS/PALSAR data. Remote Sensing Letters 4: 494–503. https://doi.org/10.1080/215070....
 
150.
Yang, J. & Warnow, T. 2011. Fast and accurate methods for phylogenomic analyses. BMC Bioinformatics 12: 4. https://doi.org/10.1186/1471-2....
 
151.
Yung, C., Chan, Y., Lacap, D. C., Pérez-Ortega, S., de Los Rios-Murillo, A., Lee, C. K., Cary, S. C. & Pointing, S. B. 2014. Characterization of chasmoendolithic community in Miers valley, McMurdo dry valleys, Antarctica. Microbial Ecology 68: 351–359. https://doi.org/10.1007/s00248....
 
152.
Zhang, T., Wang, N. & Yu, L. 2020. Soil fungal community composition differs significantly among the Antarctic, Arctic, and Tibetan Plateau. Extremophiles 24: 821–829. https://doi.org/10.1007/s00792....
 
153.
Zhou, J., Li, Z. & Guo, W. 2014. Estimation and analysis of the surface velocity field of mountain glaciers in Muztag Ata using satellite SAR data. Environmental Earth Sciences 71: 3581–3592. https://doi.org/10.1007/s12665....
 
154.
Zucconi, L., Onofri, S., Cecchini, C., Isola, D., Ripa, C., Fenice, M., Madonna, S., Reboleiro-Rivas, P. & Selbmann, L. 2016. Mapping the lithic colonization at the boundaries of life in Northern Victoria Land, Antarctica. Polar Biology 39: 91–102. https://doi.org/10.1007/s00300....
 
 
CITATIONS (1):
1.
Myrmecia, Not Asterochloris, Is the Main Photobiont of Cladonia subturgida (Cladoniaceae, Lecanoromycetes)
Raquel Pino-Bodas, Miguel Blázquez, los de, Sergio Pérez-Ortega
Journal of Fungi
 
eISSN:2657-5000
ISSN:2544-7459
Journals System - logo
Scroll to top