Research status and prospects of rock-inhabiting fungi

doi:10.17520/biods.2016140

Abstract

Abstract:

Rock-inhabiting fungi (RIF) are peculiar organisms with high diversity that apparently lack sexual reproductive structures and form compact, melanised colonies on bare rock surfaces. These fungi are one of the most stress-tolerant eukaryotic life forms on the earth and have evolved a variety of adaptive mechanisms to occupy harsh niches. They also have special characteristics related to their cell structure, metabolism, and stress tolerance mechanisms. Although RIF are very ubiquitous, they have often been overlooked due to their small size, slow growth and lack of diagnostic features. In this review, we describe the diversity, research approaches, history, adaptive mechanism and applied research of rock-inhabiting fungi, to focus attention on RIF and their importance.

Key words: rock-inhabiting fungi, diversity, stress resistance, heritage conservation, astrobiology

Shun Yang, Wei Sun, Xingzhong Liu, Meichun Xiang. Research status and prospects of rock-inhabiting fungi[J]. Biodiv Sci, 2016, 24(9): 1068-1076.

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URL: https://www.biodiversity-science.net/EN/10.17520/biods.2016140

https://www.biodiversity-science.net/EN/Y2016/V24/I9/1068

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References 98

[1]	Ascaso C, Cura GD, Ríos ADL (2004) Microbial biofilms on carbonate rocks from a quarry and monuments in Novelda (Alicante, Spain). In: Biodeterioration of Stone Surface (ed Clair LL, Seaward MRD), pp. 79-98. Kluwer Academic Publishers, Berlin.
[2]	Berbee ML, Taylor JW (1992) Detecting morphological convergence in true fungi, using 18S rRNA gene sequencing data. BioSystems, 28, 117-125.
[3]	Bogomolova EV, Minter DW (2003) A new microcolonial rock-inhabiting fungus from marble in Chersonesos (Crimea, Ukraine). Mycotaxon, 86, 195-204.
[4]	Braams J (1992) Ecological study on the fungal microflora inhabiting historical sandstone monuments. PhD thesis, University of Oldenburg, Berlin.
[5]	Cámara B, Ríos AD, Urizal M, Buergo MÁ, Varas MJ, Fort R, Ascaso C (2011) Characterizing the microbial colonization of a dolostone quarry: implications for stone biodeteriora- tion and response to biocide treatments. Microbial Ecology, 62, 299-313.
[6]	Dadachova E, Bryan RA, Huang X, Moadel T, Schweizer 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, 5, 1-13.
[7]	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.
[8]	Daghino S, Turci F, Tomatis M, Girlanda M, Fubini B, Perotto S (2009) Weathering of chrysotile asbestos by the serpentine rock-inhabiting fungus Verticillium leptobactrum. FEMS Microbiology Ecology, 69, 132-141.
[9]	De Cock AWAM (1994) Population biology of Hortaea werneckii based on restriction patterns of mitochondrial DNA. Antonie van Leeuwenhoek, 65, 21-28.
[10]	De Hoog GS (1993) Evolution of black yeasts: possible adaptation to the human host. Antonie van Leeuwenhoek, 63, 105-109.
[11]	De Hoog GS, Gueho E (1984) Deoxyribonucleic acid base composition and taxonomy of Moniliella and allied genera. Antonie van Leeuwenhoek, 50, 135-141.
[12]	De Hoog GS, Mcginnis MR (1987) Ascomycetous black yeasts. Studies in Mycology, 30, 187-199.
[13]	De Hoog GS, Zalar P, Urzì C, De Leo F, Yurlova NA, Sterflinger K (1999) Relationship of dothideaceous black yeasts and merismatic fungi based on 5.8S and ITS2 rDNA sequence comparison. Studies in Mycology, 43, 31-37.
[14]	De Leo F, Urzì C, De Hoog GS (1999) Two Coniosporium species from rock surfaces. Studies in Mycology, 43, 70-79.
[15]	De Leo F, Urzì C, De Hoog GS (2003) A new meristematic fungus, Pseudotaeniolina globosa. Antonie van Leeuwen- hoek, 83, 351-360.
[16]	Diakumaku E, Gorbushina AA, Krumbein WE, Panina L, Soukharjeski S (1995) Black fungi in marble and limestones —an aesthetical, chemical and physical problem for the conservation of monuments. The Science of the Total Environment, 167, 295-304.
[17]	Dornieden T, Gorbushina AA, Krumbein WE (1997) Änderungen der physikalischen eigenschaften von marmor durch pilzbewuchs. International Journal for Restoration of Buildings and Monuments, 3, 441-456.
[18]	Egidi E, De Hoog GS, Isola D, Onofri S, Quaedvlieg W, de Vries M, Verkley GJM, 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 Diversity, 65, 127-165.
[19]	Figueras MJ, De Hoog GS, Takeo K, Guarro J (1996) Stationary phase development of Trimmatostroma abietis. Antonie van Leeuwenhoek, 69, 217-222.
[20]	Friedmann EI (1982) Endolithic microorganisms in the Antarctic cold desert. Science, 215, 1045-1053.
[21]	Friedmann EI, Weed R (1987) Microbial trace-fossil formation, biogenous, and abiotic weathering in the Antarctic cold desert. Science, 236, 703-705.
[22]	Gadd GL, de Rome L (1988) Biosorption of copper by fungal melanin. Applied Microbiology & Biotechnology, 29, 610-617.
[23]	Gadd GM (2007) Geomycology: biogeochemical transforma- tions of rocks, minerals, metals and radionuclides by fungi, bioweathering and bioremediation. Mycological Research, 111, 3-49.
[24]	Gorbushina AA (2003) Microcolonial fungi: survival potential of terrestrial vegetative structures. Astrobiology, 3, 543-554.
[25]	Gorbushina AA (2007) Life on the rocks. Environmental Microbiology, 9, 1613-1631.
[26]	Gorbushina AA, Kotlova ER, Sherstneva OA (2008) Cellular responses of microcolonial rock fungi to long-term desicca- tion and subsequent rehydration. Studies in Mycology, 61, 91-97.
[27]	Gorbushina AA, Krumbein WK, Hamman CH, Panina L, Soukharjevski S, Wollenzien U (1993) Role of black fungi in color change and biodeterioration of antique marbles. Geomicrobiology Journal, 11, 205-221.
[28]	Gorbushina AA, Whitehead K, Dornieden T, Niesse A, Schulte A, Hedges JI (2003) Black fungal colonies as units of survival: hyphal mycosporines synthesized by rock-dwelling micro-colonial fungi. Canadian Journal of Botany, 81, 131-138.
[29]	Gravesen S, Frisvad JC, Samson RA (1994) Micro-Fungi. Damaging Effects on Building Materials. Munksgaard, Copenhagen.
[30]	Gromov BV (1957) The microflora of rocky and primitive soils in certain northern regions of USSR. Microbiology, 26, 52-59.
[31]	Gueidan C, Ruibal C, De Hoog GS, Gorbushina AA, Untere- iner WA, Lutzoni F (2008) A rock-inhabiting ancestor for mutualistic and pathogen-rich fungal lineages. Studies in Mycology, 61, 111-119.
[32]	Gueidan C, Ruibal C, De Hoog GS, Schneider H (2011) Rock-inhabiting fungi originated during periods of dry climate in the late Devonian and middle Triassic. Fungal Biology, 115, 987-996.
[33]	Gunde-Cimerman N, Zalar P, De Hoog GS, Plemenitaš A (2000) Hypersaline waters in salterns: natural ecological niches for halophilic black yeasts.Fems Microbiology Ecology, 32, 235-240.
[34]	Hawksworth DL (1991) The fungal dimension of biodiversity: magnitude, significance and conservation. Mycological Research, 95, 641-655.
[35]	Hawksworth DL (2004) Fungal diversity and its implications for genetic resource collections. Studies in Mycology, 50, 9-17.
[36]	Hawksworth DL, Rossman AY (1997) Where are all the undescribed fungi? Phytopathology, 87, 888-891.
[37]	Hofmann GE, Buckley BA, Airaksinen S, Keen JE, Somero GN (2000) Heat-shock protein expression is absent in the Antarctic fish Trematomus bernacchii (Family Notothen- iidae). Journal of Experimental Biology, 203, 2331-2339.
[38]	Hubka V, Reblova M, Rehulka J, Selbmann L, Isola D, De Hoog SG, Kolarik M (2014) Bradymyces gen. nov (Chaetothyriales, Trichomeriaceae), a new ascomycete genus accom¬modating poorly differentiated melanized fungi. Antonie van Leeuwenhoek, 106, 979-992.
[39]	Isola D, Zucconi L, Onofri S, Caneva G, De Hoog GS, Selbmann L (2016) Extremotolerant rock inhabiting black fungi from Italian monumental sites. Fungal Diversity, 76, 75-96.
[40]	Kogej T, Wheeler MH, Lanisnik-Rižner T, Gunde-Cimermann N (2003) Inhibition of DHN-melanin biosynthesis by tricyclazole in Hortaea wernekii. In: Non-conventional Yeasts in Genetics (ed Wolf K, Breunig G, Barth G), pp. 143-148. Springer, New York.
[41]	Kogej T, Wheeler MH, Rižner TL, Gunde-Cimerman N (2004) Evidence for 1,8-dihydroxy-naphthalene melanin in three halophilic black yeasts grown under saline and non-saline conditions. FEMS Microbiology Letters, 232, 203-209.
[42]	Krumbein WE, Jens K (1981) Biogenic rock varnishes of the Negev desert (Israel), an ecological study of iron and manganese transformation by cyanobacteria and fungi. Oecologia, 50, 25-38.
[43]	Ma Y, Zhang W, Xue Y (2004) Bacterial diversity of the Inner Mongolian Baer Soda Lake as revealed by 16S rRNA gene sequence analyses. Extremophiles, 8, 45-51.
[44]	Marvasi M, Donnarumma F, Frandi A, Mastromei G, Sterflin- ger K, Tiano P, Perito B (2012) Black microcolonial fungi as deteriogens of two famous marble statues in Florence, Italy.International Biodeterioration & Biodegradation Int Biodeterior Biodegrad, 68, 36-44.
[45]	Miller, RW (2005) View point: millennial fever, extreme- philes, NASA, astroenvironmentalism, and planetary pro- tection. Electronic Green Journal, 1(22)..
[46]	Minter DW (1987) The significance of conidiogenesis in pleomorphy. In: The Diversity and Its Taxonomic Implications (ed. Sugiyama J), pp. 8-11. Elsevier, Tokyo.
[47]	Muntz A (1890) Sur la décomposition des roches et la formation de la terre arable. Comptes Rendus de l’Académie des Sciences, 110, 1370-1372.
[48]	Nienow JA, Friedmann EI (1993) Terrestrial lithophytic (rock) communities. In: Antarctic Microbiology (ed. Friedmann EI), pp. 343-412. Wiley Liss, New York.
[49]	Onofri S, Barreca D, Selbmann L, Isola D, Rabbow E, Horneck G, de Vera JP, Hatton J, Zucconi L (2008) Resistance of Antarctic black fungi and cryptoendolithic communities to simulated space and Mars conditions. Studies in Mycology, 61, 99-109.
[50]	Onofri S, de la Torre R, de Vera JP, Ott S, Zucconi L, Selb- mann L, Scalzi G, Venkateswaran K, Rabbow E, Horneck G (2012) Survival of rock-colonizing organisms after 1.5 years in outer space. Astrobiology, 12, 508-516.
[51]	Onofri S, Selbmann L, Barreca D, Isola D, Zucconi L (2009) Do fungi survive under actual space conditions? Searching for evidence in favour of lithopanspermia. Plant BioSystems, 143, S85-S87.
[52]	Onofri S, Selbmann L, De Hoog GS, Grube M, Barreca D, Ruisi S, Zucconi L (2007) Evolution and adaptation of fungi at the boundaries of life. Advances in Space Research, 40, 1657-1664.
[53]	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, 148, 384-391.
[54]	Palmer FE, Staley JT, Ryan B (1990) Ecophysiology of microcolonial fungi and lichens on rocks in Northeastern Oregon. New Phytologist, 116, 613-620.
[55]	Rabbow E, Horneck G, Rettberg P, Schott JU, Panitz C, L’Afflitto A, Heise-Rotenburg R, Willnecker R, Baglioni P, Hatton J, Dettmann J, Demets R, Reitz G (2009) EXPOSE, an astrobiological exposure facility on the International Space Station—from proposal to flight. Origins of Life, 39, 581-598.
[56]	Rabbow E, Rettberg P, Barczyk S, Bohmeier M, Parpart A, Panitz C, Horneck G, von Heise-rotenburg R, Hoppenbro- uwers T, Willnecker R, Baglioni P, Demets R, Dettmann J, Reitz G (2012) EXPOSE-E: an ESA astrobiology mission 1.5 years in space. Astrobiology, 12, 374-386.
[57]	Reeb V, Roux C, Lutzoni F (2004) Contribution of RPB2 to multilocus phylogenetic studies of the euascomycetes (Pezizomycotina, Fungi) with special emphasis on the lichen-forming Acarosporaceae and evolution of polyspory. Molecular Phylogenetics and Evolution, 32, 1036-1060.
[58]	Ruibal C, Gueidan C, Selbmann L, Gorbushina AA, Crous PW, Groenewald JZ, Muggia L, Grube M, Isola D, Schoch CL, Staley JT, Lutzoni F, De Hoog GS (2009) Phylogeny of rock inhabiting fungi related to Dothideomycetes. Studies in Mycology, 64, 123-133.
[59]	Ruibal C, Platas G, Bills GF (2005) Isolation and characteriza- tion of melanized fungi from limestone formations in Mallorca. Mycological Progress , 4, 23-38.
[60]	Ruibal C, Platas G, Bills GF (2008) High diversity and morphological convergence among melanised fungi from rock formations in the Central Mountain System of Spain. Persoonia, 21, 93-110.
[61]	Schloss PD, Handelsman J (2005) Metagenomics for studying unculturable microorganisms: cutting the Gordian knot. Genome Biology, 6, 229-235.
[62]	Selbmann L, De Hoog GS, Mazzaglia A, Friedmann EI, Onofri S (2005) Fungi at the edge of life: cryptoendolithic black fungi from Antarctic desert. Studies in Mycology, 51, 1-32.
[63]	Selbmann L, De Hoog GS, Zucconi L, Isola D, Ruisi S, Gerrits AHG, Ruibal C, De Leo F, Urzì C, Onofri S (2008) Drought meets acid: three new genera in a dothidealean clade of extremotolerant fungi. Studies in Mycology, 61, 1-20
[64]	Selbmann L, Egidi E, Isola D, Onofri S, Zucconi Z, De Hoog GS, Chinaglia S, Testa L, Tosi S, Balestrazzi A, Lantieri A, Compagno R, Tigini V, Varese G (2013) Biodiversity, evolution and adaptation of fungi in extreme environments. Plant BioSystems, 147, 237-246.
[65]	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.
[66]	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.
[67]	Selbmann L, Zucconi L, Onofri S, Cecchini C, Isola D, Turchetti B, Buzzini P (2014) Taxonomic and phenotypic characterization of yeasts isolated from worldwide cold rock-associated habitats. Fungal Biology, 118, 61-71.
[68]	Sert HB, Sümbül H, Sterflinger K (2007a) Microcolonial fungi from antique marbles in Perge, Side, Termessos (Antalya, Turkey). Antonie van Leeuwenhoek, 91, 217-227.
[69]	Sert HB, Sümbül H, Sterflinger K (2007b) Sarcinomyces sideticae, a new black yeast from historical marble monuments in Side (Antalya, Turkey). Botanical Journal of the Linnean Society, 154, 373-380.
[70]	Sert HB, Sümbül H, Sterflinger K (2007c) A new species of Capnobotryella from monument surfaces. Mycological Research, 111, 1235-1241.
[71]	Staley JT, Palmer F, Adams JB (1982) Microcolonial fungi: common inhabitants on desert rocks? Science, 215, 1093-1095.
[72]	Sterflinger K (1998) Temperature and NaCl-tolerance of rock inhabiting meristematic fungi. Antonie van Leeuwenhoek, 74, 271-281.
[73]	Sterflinger K (2006) Black yeasts and meristematic fungi: ecology, diversity and identification. In: Biodiversity and Ecophysiology of Yeasts (eds Rosa C, Gabor P), pp. 505-518. Springer, New York.
[74]	Sterflinger K, de Baere R, De Hoog GS, de Watcher 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, 349-363.
[75]	Sterflinger K, De Hoog GS, Haase G (1999) Phylogeny and ecology of meristematic ascomycetes. Studies in Mycology, 43, 5-22.
[76]	Sterflinger K, Krumbein WE (1995) Multiple stress factors affecting growth of rock inhabiting black fungi. Botanica Acta, 108, 467-538.
[77]	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, e109908.
[78]	Su L, Guo LY, Hao Y, Xiang MC, Cai L, Liu XZ (2015) Rupestriomyces and Spissiomyces, two new genera of rock- inhabiting fungi from China. Mycologia, 107, 831-844.
[79]	Sterflinger K, Prillinger H (2001) Molecular taxonomy and biodiversity of rock fungal communities in an urban environment. Antonie van Leeuwenhoek, 80, 275-286.
[80]	Sterflinger K, Tesei D, Zakharova K (2012) Fungi in hot and cold deserts with particular reference to microcolonial fungi. Fungal Ecology, 5, 453-462.
[81]	Taylor-George S, Palmer F, Staley T, Borns D, Curtiss B, Adams J (1983) Fungi and bacteria involved in desert varnish formation. Microbial Ecology, 9, 227-245.
[82]	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 Biology, 116, 932-940.
[83]	Tretiach M, Bertuzzi S, Candotto F (2012) Heat shock treat- ments: a new safe approach against lichen growth on outdoor stone surfaces. Environmental Science & Technology, 46, 6851-6859.
[84]	Uijthof JMJ, De Hoog GS (1995) PCR-Ribotyping of isolates of currently accepted Exophiala and Phaeococcomyces species. Antonie van Leeuwenhoek, 68, 35-42.
[85]	Urzì C, Krumbein WE, Criseo G, Gorbushina AA, Wollenzien U (1993) Are color changes of rocks caused by climate, pollution, biological growth or by interactions of the three? In: Conservation of Stone and Other Materials (ed. Thiel MJ), pp. 279-286. Spon EFN, London.
[86]	Urzì C, Leo FD, De Hoog GS, Sterflinger K (2000) Recent advances in the molecular biology and ecophysiology of meristematic stone-inhabiting fungi. In: Of Microbes and Art (eds Ciferri O, Tiano P, Mastromei G), pp. 3-19. Springer, New York.
[87]	Van Uden N (1984) Temperature profiles of yeasts. Advances in Microbial Physiology, 25, 195-251.
[88]	Volkmann M, Whitehead K, Rütters H, Rullkötter J, Gorbushina AA (2003) Mycosporine-glutamicol-glucoside: a native UV-absorbing secondary metabolite of rock inhabi- ting microcolonial fungi (MCF). Rapid Communications in Mass Spectroscopy, 17, 897-902.
[89]	Wang J, Zhao C, Meng B (2007) The proteomic alterations of Thermoanaerobacter tengcongensis cultured at different temperatures. Proteomics, 7, 1409-1419.
[90]	Warscheid T (1990) Untersuchungen zur Biodeterioration von Sandstein unter besonderer Berücksichtigung der chemoorganotro- phen Bakterien. PhD thesis, Universität Oldenburg, Germany.
[91]	Wollenzien U, De Hoog GS, Krumbein WE, Uijthof JM (1997) Sarcinomyces petricola, a new microcolonial fungus from marble in the Mediterranean basin. Antonie van Leeuwenhoek, 71, 281-288.
[92]	Wollenzien U, De Hoog GS, Krumbein WE, Urzì 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.
[93]	Yoshida S, Takeo K, De Hoog GS, Nishimura K, Miyaji M (1996) A new type of growth exhibited by Trimmatostroma abietis. Antonie van Leeuwenhoek, 69, 211-215.
[94]	Zakharova K, Marzban G, de Vera JP, Lorek A, Sterflinger K (2014b) Protein patterns of black fungi under simulated Mars-like conditions. Scientific Reports, 4, 5114.
[95]	Zakharova K, Sterflinger K, Razzazi-Fazeli E, Noebauer K, Marzban G (2014a) Global proteomics of the extremophile black fungus Cryomyces antarcticus using 2D-Electropho- resis. Natural Science, 6, 978-995.
[96]	Zakharova K, Tesei D, Marzban G, Dijksterhuis J, Wyatt T, Sterflinger K (2013) Microcolonial fungi on rocks: a life in constant drought? Mycopathologia, 175, 537-547.
[97]	Zhdanova NN, Zakharchenko VA, Vember VV, Nakonechnaya LT (2000) Fungi from Chernobyl: mycobiota of the inner regions of the containment structures of the damaged nuclear reactor. Mycological Research, 104, 1421-1426.
[98]	Zucconi L, Gagliardi M, Isola D, Onofri S, Andaloro MC, Pelosi C, Pogliani P, Selbmann L (2012) Biodeteriorigenous agents dwelling the wall paintings of the Holy Saviour’s Cave (Vallerano, Italy). International Biodeterioration & Biodegradation, 70, 40-46.