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Review | Open Access

Rock-inhabiting fungi: terminology, diversity, evolution and adaptation mechanisms

Bingjie Liua,bRong Fua,bBing WuaXingzhong LiucMeichun Xianga,b( )
State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing, China
University of Chinese Academy of Sciences, Beijing, China
Department of Microbiology, College of Life Science, Nankai University, Tianjin, China
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Abstract

Rock-inhabiting fungi (RIF) constitute an ecological group associated with terrestrial rocks. This association is generally restricted to the persistent colonisation of rocks and peculiar morphological features based on melanisation and slow growth, which endow RIF with significance in eukaryotic biology, special status in ecology, and exotic potential in biotechnology. There is a need to achieve a better understanding of the hidden biodiversity, antistress biology, origin and convergent evolution of RIF, which will facilitate cultural relic preservation, exploitation of the biogeochemical cycle of rock elements and biotechnology applications. This review focuses on summarising the current knowledge of rock-inhabiting fungi, with particular reference to terminology, biodiversity and geographic distribution, origin and evolution, and stress adaptation mechanisms. We especially teased out the definition through summing up the terms related to rock-inhabting fungi, and also provided a checklist of rock-inhabiting fungal taxa recorded following updated classification schemes.

References

 

Abdollahzadeh J, Groenewald J, Coetzee M, Wingfield M, Crous P. 2020. Evolution of lifestyles in Capnodiales. Stud Mycol. 95:381–414. doi:10.1016/j.simyco.2020.02.004.

 

Ametrano CG, Grewe F, Crous PW, Goodwin SB, Liang C, Selbmann L, Lumbsch HT, Leavitt SD, Muggia L. 2019. Genome-scale data resolve ancestral rock-inhabiting lifestyle in Dothideomycetes (Ascomycota). IMA Fungus. 10(1):1–12. doi:10.1186/s43008-019-0018-2.

 

Araújo M, Viveiros R, Correia TR, Correia IJ, Bonifácio VD, Casimiro T, Aguiar-Ricardo A. 2014. Natural melanin: a potential pH-responsive drug release device. Int J Pharm. 469(1):140–145. doi:10.1016/j.ijpharm.2014.04.051.

 

Ascaso C, Wierzchos J, de Los Ríos A. 1995. Cytological investigations of lithobiontic microorganisms in granitic rocks. Bot Acta. 108(6):474–481. doi:10.1111/j.1438-8677.1995.tb00524.x.

 

Bentis CJ, Kaufman L, Golubic S. 2000. Endolithic fungi in reef-building corals (Order: Scleractinia) are common, cosmopolitan, and potentially pathogenic. Biol Bull. 198(2):254–260. doi:10.2307/1542528.

 

Beraldi-Campesi H. 2013. Early life on land and the first terrestrial ecosystems. Ecol Processes. 2(1):1–17.

 

Bogomolova E, Olkhovaya E, Panina L, Soukharjevsky S. 2003. Experimental study of influence of rocks and minerals chemical composition and surface structure over the lithobiontic fungi colonies morphology. Микология И Фитопатология. 37(3):1–13.

 

Breitenbach R, Silbernagl D, Toepel J, Sturm H, Broughton WJ, Sassaki GL, Gorbushina AA. 2018. Corrosive extracellular polysaccharides of the rock-inhabiting model fungus Knufia petricola. Extremophiles. 22(2):165–175. doi:10.1007/s00792-017-0984-5.

 

Bruns TD, White TJ, Taylor JW. 1991. Fungal molecular systematics. Annu Rev Ecol Syst. 22(1):525–564. doi:10.1146/annurev.es.22.110191.002521.

 

Bryan R, Jiang Z, Friedman M, Dadachova E. 2011. The effects of gamma radiation, UV and visible light on ATP levels in yeast cells depend on cellular melanization. Fungal Biol. 115(10):945–949. doi:10.1016/j.funbio.2011.04.003.

 

Caneva G, Lombardozzi V, Ceschin S, Municchia AC, Salvadori O. 2014. Unusual differential erosion related to the presence of endolithic microorganisms (Martvili, Georgia). J Cult Heritage. 15(5):538–545. doi:10.1016/j.culher.2013.10.003.

 

Caretta G, Tosi S, Piontelli E, de Hoog G. 2006. Phialophora sessilis, a lithobiont fungus. Mycotaxon. 95:281–284.

 

Casadevall A, Cordero RJ, Bryan R, Nosanchuk J, Dadachova E. 2017. Melanin, radiation, and energy transduction in fungi. Microbiol Spectr. 5(2):5.2.05. doi:10.1128/microbiolspec.FUNK-0037-2016.

 

Chertov O, Gorbushina A, Deventer B. 2004. A model for microcolonial fungi growth on rock surfaces. Ecol Modell. 177(3–4):415–426. doi:10.1016/j.ecolmodel.2004.02.011.

 

Cole BJ, Tringe SG. 2021. Different threats, same response. Nat Plants. 7(5):544–545. doi:10.1038/s41477-021-00915-z.

 

Coleine C, Masonjones S, Selbmann L, Zucconi L, Onofri S, Pacelli C, Stajich JE. 2017. Draft genome sequences of the Antarctic endolithic fungi Rachicladosporium antarcticum CCFEE 5527 and Rachicladosporium sp. CCFEE 5018. Genome Announc. 5(27):e00397–00317. doi:10.1128/genomeA.00397-17.

 

Coleine C, Masonjones S, Sterflinger K, Onofri S, Selbmann L, Stajich JE. 2020. Peculiar genomic traits in the stress-adapted cryptoendolithic Antarctic fungus Friedmanniomyces endolithicus. Fungal Biol. 124(5):458–467. doi:10.1016/j.funbio.2020.01.005.

 

Coleine C, Stajich JE, de Los Ríos A, Selbmann L. 2021. Beyond the extremes: rocks as ultimate refuge for fungi in drylands. Mycologia. 113(1):108–133. doi:10.1080/00275514.2020.1816761.

 

Coleine C, Stajich JE, Zucconi L, Onofri S, Pombubpa N, Egidi E, Franks A, Buzzini P, Selbmann L. 2018. Antarctic cryptoendolithic fungal communities are highly adapted and dominated by Lecanoromycetes and Dothideomycetes. Front Microbiol. 9:1392. doi:10.3389/fmicb.2018.01392.

 
Cooney DG, Emerson R. 1964. Thermophilic fungi. Vol. 27. San Francisco: WH Freeman.
 

Cordero RJ, Casadevall A. 2017. Functions of fungal melanin beyond virulence. Fungal Biol Rev. 31(2):99–112. doi:10.1016/j.fbr.2016.12.003.

 

Culka A, Jehlička J, Ascaso C, Artieda O, Casero CM, Wierzchos J. 2017. Raman microspectrometric study of pigments in melanized fungi from the hyperarid Atacama desert gypsum crust. J Raman Spectrosc. 48(11):1487–1493. doi:10.1002/jrs.5137.

 

Cunha MM, Franzen AJ, Seabra SH, Herbst MH, Vugman NV, Borba LP, de Souza W, Rozental S. 2010. Melanin in Fonsecaea pedrosoi: a trap for oxidative radicals. BMC Microbiol. 10(1):1–9. doi:10.1186/1471-2180-10-80.

 

Cuscó A, Catozzi C, Viñes J, Sanchez A, Francino O. 2018. Microbiota profiling with long amplicons using Nanopore sequencing: full-length 16S rRNA gene and the 16S-ITS-23S of the rrn operon. F1000Research. 7:1755. doi:10.12688/f1000research.16817.1.

 

Dadachova E, Bryan RA, Huang X, Moadel T, Schweitzer AD, Aisen P, Nosanchuk JD, Casadevall A. 2007. Ionizing radiation changes the electronic properties of melanin and enhances the growth of melanized fungi. PLoS One. 2(5):e457. doi:10.1371/journal.pone.0000457.

 

Dadachova E, Casadevall A. 2008. Ionizing radiation: how fungi cope, adapt, and exploit with the help of melanin. Curr Opin Microbiol. 11(6):525–531. doi:10.1016/j.mib.2008.09.013.

 

de Hoog GS, Hermanides-Nijhof E. 1977. The black yeasts and allied Hyphomycetes. Stud Mycol. 15:1–222.

 

de Leo F, Antonelli F, Pietrini AM, Ricci S, Urzì C. 2019. Study of the euendolithic activity of black meristematic fungi isolated from a marble statue in the Quirinale Palace’s Gardens in Rome, Italy. Facies. 65(2):1–10. doi:10.1007/s10347-019-0564-5.

 

Dornieden T, Gorbushina A, Krumbein W. 2000. Biodecay of cultural heritage as a space/time-related ecological situation—an evaluation of a series of studies. Int Biodeterior Biodegradation. 46(4):261–270. doi:10.1016/S0964-8305(00)00107-4.

 

Egidi E, de Hoog G, Isola D, Onofri S, Quaedvlieg W, de Vries M, Verkley G, Stielow JB, Zucconi L, Selbmann L. 2014. Phylogeny and taxonomy of meristematic rock-inhabiting black fungi in the Dothideomycetes based on multi-locus phylogenies. Fungal Divers. 65(1):127–165. doi:10.1007/s13225-013-0277-y.

 

Favero-Longo SE, Gazzano C, Girlanda M, Castelli D, Tretiach M, Baiocchi C, Piervittori R. 2011. Physical and chemical deterioration of silicate and carbonate rocks by meristematic microcolonial fungi and endolithic lichens (Chaetothyriomycetidae). Geomicrobiol J. 28(8):732–744. doi:10.1080/01490451.2010.517696.

 

Favero-Longo SE, Viles HA. 2020. A review of the nature, role and control of lithobionts on stone cultural heritage: weighing-up and managing biodeterioration and bioprotection. World J Microbiol Biotechnol. 36(7):1–18. doi:10.1007/s11274-020-02878-3.

 

Flieger K, Knabe N, Toepel J. 2018. Development of an improved carotenoid extraction method to characterize the carotenoid composition under oxidative stress and cold temperature in the rock inhabiting fungus Knufia petricola A95. J Fungi. 4(4):124. doi:10.3390/jof4040124.

 

Freitas DF, Vieira-Da-Motta O, Mathias LDS, Franco RWDA, Gomes RDS, Vieira RAM, Rocha LOD, Olivares FL, Santos CDP. 2019. Synthesis and role of melanin for tolerating in vitro rumen digestion in Duddingtonia flagrans, a nematode-trapping fungus. Mycology. 10(4):229–242. doi:10.1080/21501203.2019.1631896.

 

Gadd GM. 2017. Fungi, rocks, and minerals. Elements. 13(3):171–176. doi:10.2113/gselements.13.3.171.

 

Gleason FH, Larkum AW, Raven JA, Manohar CS, Lilje O. 2019. Ecological implications of recently discovered and poorly studied sources of energy for the growth of true fungi especially in extreme environments. Fungal Ecol. 39:380–387. doi:10.1016/j.funeco.2018.12.011.

 

Golubic S, Friedmann EI, Schneider J. 1981. The lithobiontic ecological niche, with special reference to microorganisms. J Sediment Res. 51(2):475–478.

 

Gonçalves V, Cantrell C, Wedge D, Alves T, Zani C, Galante D, Rodrigues F, Schaefer C, Rosa C, Rosa L. 2014. Bioprospection of rock-inhabiting fungi from extreme environments. Planta Med. 80(10): PC26. doi:10.1055/s-0034-1382408.

 

Gonçalves VN, Oliveira FS, Carvalho CR, Schaefer CE, Rosa CA, Rosa LH. 2017. Antarctic rocks from continental Antarctica as source of potential human opportunistic fungi. Extremophiles. 21(5):851–860. doi:10.1007/s00792-017-0947-x.

 

Gorbushina A. 2003. Microcolonial fungi: survival potential of terrestrial vegetative structures. Astrobiology. 3(3):543–554. doi:10.1089/153110703322610636.

 

Gorbushina AA. 2007. Life on the rocks. Environ Microbiol. 9(7):1613–1631. doi:10.1111/j.1462-2920.2007.01301.x.

 

Gorbushina AA, Andreas B, Schulte A. 2005. Microcolonial rock inhabiting fungi and lichen photobionts: evidence for mutualistic interactions. Mycol Res. 109(11):1288–1296. doi:10.1017/S0953756205003631.

 

Gorbushina AA, Broughton WJ. 2009. Microbiology of the atmosphere-rock interface: how biological interactions and physical stresses modulate a sophisticated microbial ecosystem. Annu Rev Microbiol. 63:431–450. doi:10.1146/annurev.micro.091208.073349.

 
Gorbushina AA, Krumbein WE. 2000. Rock dwelling fungal communities: diversity of life styles and colony structure. In: Seckbach, J, editor. Journey to diverse microbial worlds. Dordrecht: Springer; p. 317–334.
 

Gorbushina AA, Krumbein WE, Volkmann M. 2002. Rock surfaces as life indicators: new ways to demonstrate life and traces of former life. Astrobiology. 2(2):203–213. doi:10.1089/15311070260192273.

 

Gorbushina A, Kotlova E, Sherstneva O. 2008. Cellular responses of microcolonial rock fungi to long-term desiccation and subsequent rehydration. Stud Mycol. 61:91–97. doi:10.3114/sim.2008.61.09.

 

Gorbushina A, Krumbein W, Hamman C, Panina L, Soukharjevski S, Wollenzien U. 1993. Role of black fungi in color change and biodeterioration of antique marbles. Geomicrobiol J. 11(3–4):205–221. doi:10.1080/01490459309377952.

 

Gostinčar C, Grube M, Gunde-Cimerman N. 2011. Evolution of fungal pathogens in domestic environments? Fungal Biol. 115(10):1008–1018. doi:10.1016/j.funbio.2011.03.004.

 
Gostinčar C, Gunde‐Cimerman N, Grube M. 2015. Polyextremotolerance as the fungal answer to changing environments. In: Bakermans C, editor. Microbial evolution under extreme conditions. Berlin: de Gruyter; p. 185–208.
 

Gostinčar C, Muggia L, Grube M. 2012. Polyextremotolerant black fungi: oligotrophism, adaptive potential, and a link to lichen symbioses. Front Microbiol. 3:390. doi:10.3389/fmicb.2012.00390.

 

Gostinčar C, Stajich JE, Zupančič J, Zalar P, Gunde-Cimerman N. 2018a. Genomic evidence for intraspecific hybridization in a clonal and extremely halotolerant yeast. BMC Genomics. 19(1):1–12. doi:10.1186/s12864-018-4751-5.

 

Gostinčar C, Zajc J, Lenassi M, Plemenitaš A, de Hoog S, Al-Hatmi AM, Gunde-Cimerman N. 2018b. Fungi between extremotolerance and opportunistic pathogenicity on humans. Fungal Divers. 93(1):195–213. doi:10.1007/s13225-018-0414-8.

 

Gromov B. 1957. Microflora of rocky and primitive soils in certain northern regions of USSR. Mikrobiologiia. 26(1):52–59.

 
Grube M, Muggia L, Gostinčar C. 2013. Niches and adaptations of polyextremotolerant black fungi. In: Seckbach, J, Oren, A, and Stan-Lotter, H, editors. Polyextremophiles. Dordrecht: Springer; p. 551–566.
 

Gueidan C, Ruibal C, de Hoog G, Schneider H. 2011. Rock-inhabiting fungi originated during periods of dry climate in the late Devonian and middle Triassic. Fungal Biol. 115(10):987–996. doi:10.1016/j.funbio.2011.04.002.

 

Gueidan C, Villaseñor CR, de Hoog G, Gorbushina A, Untereiner W, Lutzoni F. 2008. A rock-inhabiting ancestor for mutualistic and pathogen-rich fungal lineages. Stud Mycol. 61:111–119. doi:10.3114/sim.2008.61.11.

 

Heinen W, Lauwers A. 1986. Mold on the rocks: a lithobiontic fungus from the sediments of radioactive thermal waters in the Gastein Valley, Austria. Acta Bot Neerl. 35(3):367–372. doi:10.1111/j.1438-8677.1986.tb01299.x.

 

Hubka V, Réblová M, Řehulka J, Selbmann L, Isola D, de Hoog SG, Kolařík M. 2014. Bradymyces gen. nov. (Chaetothyriales, Trichomeriaceae), a new ascomycete genus accommodating poorly differentiated melanized fungi. Antonie van Leeuwenhoek. 106(5):979–992. doi:10.1007/s10482-014-0267-4.

 

Isola D, Marzban G, Selbmann L, Onofri S, Laimer M, Sterflinger K. 2011. Sample preparation and 2-DE procedure for protein expression profiling of black microcolonial fungi. Fungal Biol. 115(10):971–977. doi:10.1016/j.funbio.2011.03.001.

 

Isola D, Selbmann L, de Hoog GS, Fenice M, Onofri S, Prenafeta-Boldú FX, Zucconi L. 2013. Isolation and screening of black fungi as degraders of volatile aromatic hydrocarbons. Mycopathologia. 175(5–6):369–379. doi:10.1007/s11046-013-9635-2.

 

Isola D, Zucconi L, Onofri S, Caneva G, de Hoog G, Selbmann L. 2016. Extremotolerant rock inhabiting black fungi from Italian monumental sites. Fungal Divers. 76(1):75–96. doi:10.1007/s13225-015-0342-9.

 

King Jr AD, Hocking AD, Pitt JI. 1979. Dichloran-rose bengal medium for enumeration and isolation of molds from foods. Appl Environ Microbiol. 37(5):959–964. doi:10.1128/aem.37.5.959-964.1979.

 

Kirtzel J, Siegel D, Krause K, Kothe E. 2017. Stone-eating fungi: mechanisms in bioweathering and the potential role of laccases in black slate degradation with the basidiomycete Schizophyllum commune. Adv Appl Microbiol. 99:83–101.

 

Kiyuna T, An K-D, Kigawa R, Sano C, Sugiyama J. 2018. Two new Cladophialophora species, C. tumbae sp. nov. and C. tumulicola sp. nov., and chaetothyrialean fungi from biodeteriorated samples in the Takamatsuzuka and Kitora Tumuli. Mycoscience. 59(1):75–84. doi:10.1016/j.myc.2017.08.008.

 

Kuklinski P. 2009. Ecology of stone-encrusting organisms in the Greenland Sea—a review. Polar Res. 28(2):222–237. doi:10.1111/j.1751-8369.2009.00105.x.

 
Lakk H, Krijgsheld P, Montalti M, Woesten H 2018. Fungal based biocomposite for habitat structures on the moon and mars. 69th International Astronautical Congress Bremen, Germany.
 

Lenassi M, Gostinčar C, Jackman S, Turk M, Sadowski I, Nislow C, Jones S, Birol I, Cimerman NG, Plemenitaš A. 2013. Whole genome duplication and enrichment of metal cation transporters revealed by de novo genome sequencing of extremely halotolerant black yeast Hortaea werneckii. PLoS One. 8(8):e71328. doi:10.1371/journal.pone.0071328.

 

Liberti D, Alfieri ML, Monti DM, Panzella L, Napolitano A. 2020. A melanin-related phenolic polymer with potent photoprotective and antioxidant activities for dermo-cosmetic applications. Antioxidants. 9(4):270. doi:10.3390/antiox9040270.

 

Luo Y, Wei X, Yang S, Gao Y-H, Luo Z-H. 2020. Fungal diversity in deep-sea sediments from the Magellan seamounts as revealed by a metabarcoding approach targeting the ITS2 regions. Mycology. 11(3):214–229. doi:10.1080/21501203.2020.1799878.

 

Lyu X, Shen C, Xie J, Fu Y, Jiang D, Hu Z, Tang L, Tang L, Ding F, Li K. 2015. A “footprint” of plant carbon fixation cycle functions during the development of a heterotrophic fungus. Sci Rep. 5(1):1–13. doi:10.1038/srep12952.

 

Martin-Sanchez PM, Nováková A, Bastian F, Alabouvette C, Saiz-Jimenez C. 2012. Two new species of the genus Ochroconis, O. lascauxensis and O. anomala isolated from black stains in Lascaux Cave, France. Fungal Biol. 116(5):574–589. doi:10.1016/j.funbio.2012.02.006.

 

Mikhailyuk TI. 2008. Terrestrial lithophilic algae in a granite canyon of the Teteriv River (Ukraine). Biologia. 63(6):824–830. doi:10.2478/s11756-008-0104-1.

 

Miura A, Urabe J. 2017. Changes in epilithic fungal communities under different light conditions in a river: a field experimental study. Limnol Oceanogr. 62(2):579–591. doi:10.1002/lno.10445.

 

Moreno LF, Vicente VA, de Hoog S. 2018. Black yeasts in the omics era: achievements and challenges. Med Mycol. 56(suppl_1):S32–S41. doi:10.1093/mmy/myx129.

 

Nagano Y, Miura T, Tsubouchi T, Lima AO, Kawato M, Fujiwara Y, Fujikura K. 2020. Cryptic fungal diversity revealed in deep-sea sediments associated with whale-fall chemosynthetic ecosystems. Mycology. 11(3):263–278. doi:10.1080/21501203.2020.1799879.

 
Nai C. 2014. Rock-inhabiting fungi studied with the aid of the model black fungus Knufia petricola A95 and other related strains. Bundesanstalt für Materialforschung und-prüfung (BAM).
 

Nai C, Wong HY, Pannenbecker A, Broughton WJ, Benoit I, de Vries RP, Gueidan C, Gorbushina AA. 2013. Nutritional physiology of a rock-inhabiting, model microcolonial fungus from an ancestral lineage of the Chaetothyriales (Ascomycetes). Fungal Genet Biol. 56:54–66. doi:10.1016/j.fgb.2013.04.001.

 

Naranjo‐Ortiz MA, Gabaldón T. 2019. Fungal evolution: major ecological adaptations and evolutionary transitions. Biol Rev. 94(4):1443–1476. doi:10.1111/brv.12510.

 

Noack-Schönmann S, Bus T, Banasiak R, Knabe N, Broughton WJ, Den Dulk-Ras H, Hooykaas PJ, Gorbushina AA. 2014. Genetic transformation of Knufia petricola A95-a model organism for biofilm-material interactions. AMB Express. 4(1):1–6. doi:10.1186/s13568-014-0080-5.

 

Noack-Schönmann S, Spagin O, Gründer K-P, Breithaupt M, Günter A, Muschik B, Gorbushina A. 2014b. Sub-aerial biofilms as blockers of solar radiation: spectral properties as tools to characterise material-relevant microbial growth. Int Biodeterior Biodegradation. 86:286–293. doi:10.1016/j.ibiod.2013.09.020.

 

Omelon CR. 2008. Endolithic microbial communities in polar desert habitats. Geomicrobiol J. 25(7–8):404–414. doi:10.1080/01490450802403057.

 

Onofri S, Barreca D, Selbmann L, Isola D, Rabbow E, Horneck G, de Vera J, Hatton J, Zucconi L. 2008. Resistance of Antarctic black fungi and cryptoendolithic communities to simulated space and Martian conditions. Stud Mycol. 61:99–109. doi:10.3114/sim.2008.61.10.

 

Onofri S, de La Torre R, de Vera J-P, Ott S, Zucconi L, Selbmann L, Scalzi G, Venkateswaran KJ, Rabbow E, Sánchez Iñigo FJ. 2012. Survival of rock-colonizing organisms after 1.5 years in outer space. Astrobiology. 12(5):508–516. doi:10.1089/ast.2011.0736.

 

Onofri S, de Vera J-P, Zucconi L, Selbmann L, Scalzi G, Venkateswaran KJ, Rabbow E, de La Torre R, Horneck G. 2015. Survival of Antarctic cryptoendolithic fungi in simulated Martian conditions on board the International Space Station. Astrobiology. 15(12):1052–1059. doi:10.1089/ast.2015.1324.

 

Onofri S, Selbmann L, de Hoog G, Grube M, Barreca D, Ruisi S, Zucconi L. 2007. Evolution and adaptation of fungi at boundaries of life. Adv Space Res. 40(11):1657–1664. doi:10.1016/j.asr.2007.06.004.

 

Onofri S, Selbmann L, Pacelli C, de Vera JP, Horneck G, Hallsworth JE, Zucconi L. 2018. Integrity of the DNA and cellular ultrastructure of cryptoendolithic fungi in space or Mars conditions: a 1.5-year study at the International Space Station. Life. 8(2):23. doi:10.3390/life8020023.

 

Onofri S, Selbmann L, Zucconi L, Pagano S. 2004. Antarctic microfungi as models for exobiology. Planet Space Sci. 52(1–3):229–237. doi:10.1016/j.pss.2003.08.019.

 

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 Biosyst. 148(2):384–391. doi:10.1080/11263504.2013.877533.

 

Pacelli C, Bryan RA, Onofri S, Selbmann L, Shuryak I, Dadachova E. 2017a. Melanin is effective in protecting fast and slow growing fungi from various types of ionizing radiation. Environ Microbiol. 19(4):1612–1624. doi:10.1111/1462-2920.13681.

 

Pacelli C, Bryan RA, Onofri S, Selbmann L, Zucconi L, Shuryak I, Dadachova E. 2018a. The effect of protracted X‐ray exposure on cell survival and metabolic activity of fast and slow growing fungi capable of melanogenesis. Environ Microbiol Rep. 10(3):255–263. doi:10.1111/1758-2229.12632.

 

Pacelli C, Bryan RA, Onofri S, Selbmann L, Zucconi L, Shuryak I, Dadachova E. 2018b. Survival and redox activity of Friedmanniomyces endolithicus, an Antarctic endemic black meristematic fungus, after gamma rays exposure. Fungal Biol. 122(12):1222–1227. doi:10.1016/j.funbio.2018.10.002.

 

Pacelli C, Cassaro A, Maturilli A, Timperio AM, Gevi F, Cavalazzi B, Stefan M, Ghica D, Onofri S. 2020. Multidisciplinary characterization of melanin pigments from the black fungus Cryomyces antarcticus. Appl Microbiol Biotechnol. 104:6385–6395. doi:10.1007/s00253-020-10666-0.

 

Pacelli C, Selbmann L, Zucconi L, Coleine C, de Vera J-P, Rabbow E, Böttger U, Dadachova E, Onofri S. 2019. Responses of the black fungus cryomyces antarcticus to simulated Mars and space conditions on rock analogs. Astrobiology. 19(2):209–220. doi:10.1089/ast.2016.1631.

 

Pacelli C, Selbmann L, Zucconi L, de Vera J-P, Rabbow E, Horneck G, de La Torre R, Onofri S. 2017b. BIOMEX experiment: ultrastructural alterations, molecular damage and survival of the fungus Cryomyces antarcticus after the experiment verification tests. Origins Life Evol Biospheres. 47(2):187–202. doi:10.1007/s11084-016-9485-2.

 

Pacelli C, Selbmann L, Zucconi L, Raguse M, Moeller R, Shuryak I, Onofri S. 2017c. Survival, DNA integrity, and ultrastructural damage in Antarctic cryptoendolithic eukaryotic microorganisms exposed to ionizing radiation. Astrobiology. 17(2):126–135. doi:10.1089/ast.2015.1456.

 

Palmer F, Emery D, Stemmler J, Staley J. 1987. Survival and growth of microcolonial rock fungi as affected by temperature and humidity. New Phytol. 107(1):155–162. doi:10.1111/j.1469-8137.1987.tb04889.x.

 

Palmer F, Staley J, Ryan B. 1990. Ecophysiology of microcolonial fungi and lichens on rocks in Northeastern Oregon. New Phytol. 116(4):613–620. doi:10.1111/j.1469-8137.1990.tb00546.x.

 

Palmer R, Friedmann E. 1988. 2.9 incorporation of inorganic carbon by Antarctic cryptoendolithic fungi. Polarforschung. 58(2/3):189–191.

 
Perry RS, Gorbushina A, Engel MH, Kolb VM, Krumbein WE, Staley JT. 2004. Accumulation and deposition of inorganic and organic compounds by microcolonial fungi. Third European Workshop on Exo-Astrobiology Madrid, Spain.
 

Pinheiro AC, Mesquita N, Trovão J, Soares F, Tiago I, Coelho C, de Carvalho HP, Gil F, Catarino L, Piñar G. 2019. Limestone biodeterioration: a review on the Portuguese cultural heritage scenario. J Cult Heritage. 36:275–285. doi:10.1016/j.culher.2018.07.008.

 

Pombeiro-Sponchiado SR, Sousa GS, Andrade JC, Lisboa HF, Gonçalves RC. 2017. Production of melanin pigment by fungi and its biotechnological applications. Melanin. 47–75.

 

Prenafeta-Boldú FX, Roca N, Villatoro C, Vera L, de Hoog GS. 2019. Prospective application of melanized fungi for the biofiltration of indoor air in closed bioregenerative systems. J Hazard Mater. 361:1–9. doi:10.1016/j.jhazmat.2018.08.059.

 

Réblová M, Hubka V, Thureborn O, Lundberg J, Sallstedt T, Wedin M, Ivarsson M. 2016. From the tunnels into the treetops: new lineages of black yeasts from biofilm in the Stockholm metro system and their relatives among ant-associated fungi in the Chaetothyriales. PLoS One. 11(10):e0163396. doi:10.1371/journal.pone.0163396.

 

Revankar SG. 2007. Dematiaceous fungi. Mycoses. 50(2):91–101. doi:10.1111/j.1439-0507.2006.01331.x.

 

Revankar SG, Sutton DA. 2010. Melanized fungi in human disease. Clin Microbiol Rev. 23(4):884–928. doi:10.1128/CMR.00019-10.

 

Ruibal C, Gueidan C, Selbmann L, Gorbushina A, Crous P, Groenewald J, Muggia L, Grube M, Isola D, Schoch C. 2009. Phylogeny of rock-inhabiting fungi related to Dothideomycetes. Stud Mycol. 64:123–133. doi:10.3114/sim.2009.64.06.

 

Ruibal C, Platas G, Bills G. 2008. High diversity and morphological convergence among melanised fungi from rock formations in the Central Mountain System of Spain. Persoonia. 21:93. doi:10.3767/003158508X371379.

 

Ruibal C, Platas G, Bills GF. 2005. Isolation and characterization of melanized fungi from limestone formations in Mallorca. Mycol Prog. 4(1):23–38. doi:10.1007/s11557-006-0107-7.

 

Ruibal C, Selbmann L, Avci S, Martin-Sanchez PM, Gorbushina AA. 2018. Roof-inhabiting cousins of rock-inhabiting fungi: novel melanized microcolonial fungal species from photocatalytically reactive subaerial surfaces. Life. 8(3):30. doi:10.3390/life8030030.

 

Scalzi G, Selbmann L, Zucconi L, Rabbow E, Horneck G, Albertano P, Onofri S. 2012. LIFE experiment: isolation of cryptoendolithic organisms from Antarctic colonized sandstone exposed to space and simulated Mars conditions on the International Space Station. Origins Life Evol Biospheres. 42(2):253–262. doi:10.1007/s11084-012-9282-5.

 

Scheerer S, Ortega‐Morales O, Gaylarde C. 2009. Microbial deterioration of stone monuments—an updated overview. Adv Appl Microbiol. 66:97–139.

 

Schumacher J, Gorbushina AA. 2020. Light sensing in plant-and rock-associated black fungi. Fungal Biol. 124(5):407–417. doi:10.1016/j.funbio.2020.01.004.

 

Seiffert F, Bandow N, Bouchez J, Von Blanckenburg F, Gorbushina A. 2014. Microbial colonization of bare rocks: laboratory biofilm enhances mineral weathering. Procedia Earth Planet Sci. 10:123–129. doi:10.1016/j.proeps.2014.08.042.

 

Selbmann L, Benkő Z, Coleine C, de Hoog S, Donati C, Druzhinina I, Emri T, Ettinger CL, Gladfelter AS, Gorbushina AA, et al. 2020. Shed light in the DaRk LineagES of the fungal tree of life—STRES[J]. Life. 10(12):362. doi:10.3390/life10120362.

 

Selbmann L, de Hoog G, Mazzaglia A, Friedmann E, Onofri S. 2005. Fungi at the edge of life: cryptoendolithic black fungi from Antarctic desert. Stud Mycol. 51(1):1–32.

 

Selbmann L, de Hoog G, Zucconi L, Isola D, Ruisi S, van Den Ende AG, Ruibal C, de Leo F, Urzì C, Onofri S. 2008. Drought meets acid: three new genera in a dothidealean clade of extremotolerant fungi. Stud Mycol. 61:1–20. doi:10.3114/sim.2008.61.01.

 

Selbmann L, Grube M, Onofri S, Isola D, Zucconi L. 2013. Antarctic epilithic lichens as niches for black meristematic fungi. Biology. 2(2):784–797. doi:10.3390/biology2020784.

 

Selbmann L, Isola D, Egidi E, Zucconi L, Gueidan C, de Hoog G, Onofri S. 2014. Mountain tips as reservoirs for new rock-fungal entities: saxomyces gen. nov. and four new species from the Alps. Fungal Divers. 65(1):167–182. doi:10.1007/s13225-013-0234-9.

 

Selbmann L, Pacelli C, Zucconi L, Dadachova E, Moeller R, de Vera J-P, Onofri S. 2018. Resistance of an Antarctic cryptoendolithic black fungus to radiation gives new insights of astrobiological relevance. Fungal Biol. 122(6):546–554. doi:10.1016/j.funbio.2017.10.012.

 

Selbmann L, Zucconi L, Isola D, Onofri S. 2015. Rock black fungi: excellence in the extremes, from the Antarctic to space. Curr Genet. 61(3):335–345. doi:10.1007/s00294-014-0457-7.

 

Sert HB, Sterflinger K. 2010. A new Coniosporium species from historical marble monuments. Mycol Prog. 9(3):353–359. doi:10.1007/s11557-009-0643-z.

 

Sert HB, Suembuel H, Sterflinger K. 2007a. A new species of Capnobotryella from monument surfaces. Mycol Res. 111(10):1235–1241. doi:10.1016/j.mycres.2007.06.011.

 

Sert HB, Suembuel H, Sterflinger K. 2007b. Sarcinomyces sideticae, a new black yeast from historical marble monuments in Side (Antalya, Turkey). Bot J Linn Soc. 154(3):373–380. doi:10.1111/j.1095-8339.2007.00658.x.

 

Sert HB, Suembuel H, Sterflinger K. 2011. Two new species of Capnobotryella from historical monuments. Mycol Prog. 10(3):333–339. doi:10.1007/s11557-010-0706-1.

 

Sert HB, Wuczkowski M, Sterflinger K. 2012. Capnobotryella isiloglui, a new rock-inhabiting fungus from Austria. Turk J Bot. 36(4):401–407.

 

Shirakawa MA, Zilles R, Mocelin A, Gaylarde CC, Gorbushina A, Heidrich G, Giudice MC, Del Negro GM, John VM. 2015. Microbial colonization affects the efficiency of photovoltaic panels in a tropical environment. J Environ Manage. 157:160–167. doi:10.1016/j.jenvman.2015.03.050.

 

Silva-Bailao MG, Da Silva KLP, Dos Anjos LRB, de Sousa Lima P, de Melo Teixeira M, de Almeida Soares CM, Bailão AM. 2018. Mechanisms of copper and zinc homeostasis in pathogenic black fungi. Fungal Biol. 122(6):526–537. doi:10.1016/j.funbio.2017.12.002.

 
Singleton I, Tobin JM. 1996. Fungal interactions with metals and radionuclides for environmental bioremediation. Fungi and environmental change: symposium of the British Mycological Society, held at Cranfield University; March 1994. Cambridge [England]; New York: Published for the British Mycological Society ….
 
Smith DF, Casadevall A. 2019. The role of melanin in fungal pathogenesis for animal hosts. In: Rodrigues, M, editor. Fungal physiology and immunopathogenesis. Cham: Springer; p. 1–30.
 

Staley JT, Palmer F, Adams JB. 1982. Microcolonial fungi: common inhabitants on desert rocks? Science. 215(4536):1093–1095. doi:10.1126/science.215.4536.1093.

 

Sterflinger K. 1998a. Ecophysiology of rock inhabiting black yeasts with special reference to temperature and osmotic stress. Antonie van Leeuwenhoek. 74:271–281. doi:10.1023/A:1001753131034.

 

Sterflinger K. 1998b. Temperature and NaCl-tolerance of rock-inhabiting meristematic fungi. Antonie van Leeuwenhoek. 74(4):271–281.

 

Sterflinger K, de Baere R, de Hoog G, de Wachter R, Krumbein WE, Haase G. 1997. Coniosporium perforans and C. apollinis, two new rock-inhabiting fungi isolated from marble in the Sanctuary of Delos (Cyclades, Greece). Antonie van Leeuwenhoek. 72(4):349–363. doi:10.1023/A:1000570429688.

 

Sterflinger K, de Hoog G, Haase G. 1999. Phylogeny and ecology of meristematic ascomycetes. Stud Mycol. 43:5–22.

 

Sterflinger K, Gorbushina AA. 1997. Morphological and molecular characterization of a rock inhabiting and rock decaying dematiaceous fungus isolated from antique monuments of Delos (Cyclades, Greece) and Chersonesus (Crimea, Ukraine). Syst Appl Microbiol. 20(2):329–335. doi:10.1016/S0723-2020(97)80080-X.

 

Sterflinger K, Hain M. 1999. In situ hybridization with rRNA targeted probes as a new tool for the detection of black yeasts and meristematic fungi. Stud Mycol. 43:23–30.

 

Sterflinger K, Krumbein W. 1995. Multiple stress factors affecting growth of rock‐inhabiting black fungi. Bot Acta. 108(6):490–496. doi:10.1111/j.1438-8677.1995.tb00526.x.

 

Sterflinger K, Lopandic K, Pandey RV, Blasi B, Kriegner A. 2014. Nothing special in the specialist? Draft genome sequence of Cryomyces antarcticus, the most extremophilic fungus from Antarctica. PLoS One. 9(10):e109908. doi:10.1371/journal.pone.0109908.

 
Sterflinger K. 2006. Black yeasts and meristematic fungi: ecology, diversity and identification. In: Péter, G, Rosa, C, editors. Biodiversity and ecophysiology of yeasts. Berlin, Heidelberg: Springer; p. 501–514.
 

Sterflinger K, Piñar G. 2013. Microbial deterioration of cultural heritage and works of art—tilting at windmills? Appl Microbiol Biotechnol. 97(22):9637–9646. doi:10.1007/s00253-013-5283-1.

 

Sterflinger K, Tesei D, Zakharova K. 2012. Fungi in hot and cold deserts with particular reference to microcolonial fungi. Fungal Ecol. 5(4):453–462. doi:10.1016/j.funeco.2011.12.007.

 

Su C-J, Hsieh S-Y, Chiang MW-L, Pang K-L. 2020. Salinity, pH and temperature growth ranges of Halophytophthora isolates suggest their physiological adaptations to mangrove environments. Mycology. 11(3):256–262. doi:10.1080/21501203.2020.1714768.

 

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(4):831–844. doi:10.3852/14-305.

 

Sun W, Liu B, Fu R, Liu X, Xiang M. 2019. Two new rock-inhabiting species of Cyphellophora from karst habitats in China. Phytotaxa. 397(1):23–33. doi:10.11646/phytotaxa.397.1.2.

 

Sun W, Su L, Yang S, Sun J, Liu B, Fu R, Wu B, Liu X, Cai L, Guo L. 2020. Unveiling the hidden diversity of rock-inhabiting fungi: chaetothyriales from China. J Fungi. 6(4):187. doi:10.3390/jof6040187.

 

Taylor JW, Jacobson DJ, Kroken S, Kasuga T, Geiser DM, Hibbett DS, Fisher MC. 2000. Phylogenetic species recognition and species concepts in fungi. Fungal Genet Biol. 31(1):21–32. doi:10.1006/fgbi.2000.1228.

 

Teixeira M, Moreno LF, Stielow B, Muszewska A, Hainaut M, Gonzaga L, Abouelleil A, Patané J, Priest M, Souza R. 2017. Exploring the genomic diversity of black yeasts and relatives (Chaetothyriales, Ascomycota). Stud Mycol. 86:1–28. doi:10.1016/j.simyco.2017.01.001.

 

Tesei D, Marzban G, Zakharova K, Isola D, Selbmann L, Sterflinger K. 2012. Alteration of protein patterns in black rock inhabiting fungi as a response to different temperatures. Fungal Biol. 116(8):932–940. doi:10.1016/j.funbio.2012.06.004.

 

Tesei D, Quartinello F, Guebitz GM, Ribitsch D, Nöbauer K, Razzazi-Fazeli E, Sterflinger K. 2020. Shotgun proteomics reveals putative polyesterases in the secretome of the rock-inhabiting fungus Knufia chersonesos. Sci Rep. 10(1):1–15. doi:10.1038/s41598-019-56847-4.

 

Tonon C, Breitenbach R, Voigt O, Turci F, Gorbushina AA, Favero-Longo SE. 2021. Hyphal morphology and substrate porosity-rather than melanization-drive penetration of black fungi into carbonate substrates. J Cult Heritage. 48:244–253. doi:10.1016/j.culher.2020.11.003.

 

Trovão J, Tiago I, Soares F, Paiva DS, Mesquita N, Coelho C, Catarino L, Gil F, Portugal A. 2019. Description of Aeminiaceae fam. nov., Aeminium gen. nov. and Aeminiumludgeri sp. nov. (Capnodiales), isolated from a biodeteriorated art-piece in the Old Cathedral of Coimbra, Portugal. MycoKeys. (45):57. doi:10.3897/mycokeys.45.31799.

 
Urzì C, de Leo F, de Hoog S, Sterflinger K. 2000. Recent advances in the molecular biology and ecophysiology of meristematic stone-inhabiting fungi. In: Ciferri, O, Tiano, P, Mastromei, G, editors. Of microbes and art. Boston (MA): Springer; p. 3–19 doi:10.1007/978-1-4615-4239-1_1.
 

Urzì C, Wollenzien U, Criseo G, Krumbein WE. 1995. Biodiversity of the rock inhabiting microflora with special reference to black fungi and black yeasts. Microbial diversity and ecosystem function. 16:289–302

 

Vahidzadeh E, Kalra AP, Shankar K. 2018. Melanin-based electronics: from proton conductors to photovoltaics and beyond. Biosens Bioelectron. 122:127–139. doi:10.1016/j.bios.2018.09.026.

 

Vasileiou T, Summerer L. 2020. A biomimetic approach to shielding from ionizing radiation: the case of melanized fungi. PLoS One. 15(4):e0229921. doi:10.1371/journal.pone.0229921.

 

Vázquez-Nion D, Rodríguez-Castro J, López-Rodríguez M, Fernández-Silva I, Prieto B. 2016. Subaerial biofilms on granitic historic buildings: microbial diversity and development of phototrophic multi-species cultures. Biofouling. 32(6):657–669. doi:10.1080/08927014.2016.1183121.

 

Voigt O, Knabe N, Nitsche S, Erdmann EA, Schumacher J, Gorbushina AA. 2020. An advanced genetic toolkit for exploring the biology of the rock-inhabiting black fungus Knufia petricola. Sci Rep. 10(1):1–14. doi:10.1038/s41598-020-79120-5.

 

Volkmann M, Whitehead K, Rütters H, Rullkötter J, Gorbushina AA. 2003. Mycosporine‐glutamicol‐glucoside: a natural UV‐absorbing secondary metabolite of rock‐inhabiting microcolonial fungi. Rapid Commun Mass Spectrom. 17(9):897–902. doi:10.1002/rcm.997.

 

Wollenzien U, de Hoog G, Krumbein W, Uijthof J. 1997. Sarcinomyces petricola, a new microcolonial fungus from marble in the Mediterranean basin. Antonie van Leeuwenhoek. 71(3):281–288. doi:10.1023/A:1000157803954

 

Wollenzien U, de Hoog G, Krumbein W, Urzi C. 1995. On the isolation of microcolonial fungi occurring on and in marble and other calcareous rocks. Sci Total Environ. 167(1–3):287–294. doi:10.1016/0048-9697(95)04589-S.

 

Wu B, Hussain M, Zhang W, Stadler M, Liu X, Xiang M. 2019. Current insights into fungal species diversity and perspective on naming the environmental DNA sequences of fungi. Mycology. 10(3):127–140. doi:10.1080/21501203.2019.1614106.

 

Zakharova K, Marzban G, de Vera J-P, Lorek A, Sterflinger K. 2014. Protein patterns of black fungi under simulated Mars-like conditions. Sci Rep. 4(1):1–7.

 

Zakharova K, Tesei D, Marzban G, Dijksterhuis J, Wyatt T, Sterflinger K. 2013. Microcolonial fungi on rocks: a life in constant drought? Mycopathologia. 175(5–6):537–547. doi:10.1007/s11046-012-9592-1.

 
Zhang Z-F, Pan Y-P, Liu Y, Li M. 2020. Pacific Biosciences Single-molecule Real-time (SMRT) Sequencing reveals high diversity of basal fungal lineages and stochastic processes controlled fungal community assembly in mangrove sediments.
Mycology
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Cite this article:
Liu B, Fu R, Wu B, et al. Rock-inhabiting fungi: terminology, diversity, evolution and adaptation mechanisms. Mycology, 2022, 13(1): 1-31. https://doi.org/10.1080/21501203.2021.2002452

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Received: 10 August 2021
Accepted: 30 October 2021
Published: 27 December 2021
© 2021 The Author(s).

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