The haustorium as a driving force for speciation in thallus-forming Laboulbeniomycetes

. 2022 Jan 31 ; 13 (1) : 1. [epub] 20220131

Status PubMed-not-MEDLINE Jazyk angličtina Země Velká Británie, Anglie Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid35101145

Grantová podpora
1206620N Fonds Wetenschappelijk Onderzoek
SYNTHESYS+ grant no. BE-TAF-151 horizon 2020

Odkazy

PubMed 35101145
PubMed Central PMC8805332
DOI 10.1186/s43008-021-00087-7
PII: 10.1186/s43008-021-00087-7
Knihovny.cz E-zdroje

Laboulbeniomycetes is a class of fungi that have obligate associations with arthropod hosts, either for dispersal (order Pyxidiophorales) or as biotrophic parasites (orders Herpomycetales and Laboulbeniales). Here, we focus on Herpomycetales and Laboulbeniales, which include fungi that form thalli, 3-dimensional, multicellular units of 1000 s of cells. Based on recently published data regarding patterns of speciation, we present the One-Host-One-Parasite model (1H1P) for haustorial thallus-forming Laboulbeniomycetes. We hypothesize that taxa with haustoria, rhizoidal structures that make contact with the host's body cavity, have very strict host specificity. For taxa without haustoria, the microhabitat-as selected by the host-governs host shifting, presence or absence of the fungus, abundance, effective host range, and geographic distribution. We make suggestions for future research including fluorescent labeling of waxy lipids and mass spectrometry. These techniques have the potential to generate the data necessary to evaluate the here proposed 1H1P hypothesis for Herpomycetales and Laboulbeniales.

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Accioly T, Sousa JO, Moreau PA, Lécuru C, Silva BD, Roy M, Gardes M, Baseia IG, Martín MP. Hidden fungal diversity from the Neotropics: Geastrum hirsutum, G. schweinitzii (Basidiomycota, Geastrales) and their allies. PLoS ONE. 2019;14(2):e0211388. doi: 10.1371/journal.pone.0211388. PubMed DOI PMC

Aime MC, Miller AN, Aoki T, Bensch K, Cai L, Crous PW, Hawksworth DL, Hyde KD, Kirk PM, Lücking R, May TW, Malosso E, Redhead SA, Rossman AY, Stadler M, Thines M, Yurkov AM, Zhang N, Schoch CL. How to publish a new fungal species, or name, version 3.0. IMA Fungus. 2021;12(1):11. doi: 10.1186/s43008-021-00063-1. PubMed DOI PMC

Araújo JPM, Evans HC, Kepler R, Hughes DP. Zombie- ant fungi across continents: 15 new species and new combinations within Ophiocordyceps. I. Myrmecophilous Hirsutelloid Species. Stud Mycol. 2018;90:119–160. doi: 10.1016/j.simyco.2017.12.002. PubMed DOI PMC

Benjamin RK. Introduction and supplement to Roland Thaxter's contribution towards a monograph of the Laboulbeniaceae. Bibl Mycol. 1971;30:1–155.

Benjamin RK, Shanor L. Sex of host specificity and position specificity of certain species of Laboulbenia on Bembidion picipes. Am J Bot. 1952;39(2):125–131. doi: 10.1002/j.1537-2197.1952.tb14255.x. DOI

Blackwell M, Malloch D. Pyxidiophora: Life histories and arthropod associations of two species. Can J Bot. 1989;67(9):2552–2562. doi: 10.1139/b89-330. DOI

Blackwell M, Bridges JR, Moser JC, Perry TJ. Hyperphoretic dispersal of a Pyxidiophora anamorph. Science. 1986;232(4753):993–995. doi: 10.1126/science.232.4753.993. PubMed DOI

Blackwell M, Perry TJ, Bridges JR, Moser JC. A new species of Pyxidiophora and its Thaxteriola anamorph. Mycologia. 1986;78(4):607–614. doi: 10.2307/3807773. DOI

Blackwell M, Haelewaters D, Pfister DH. Evolution, natural history, and Thaxter’s final word. Mycologia. 2020;112(6):1048–1059. doi: 10.1080/00275514.2020.1718442. PubMed DOI

Cao B, Haelewaters D, Schoutteten N, Begerow D, Boekhout T, Giachini AJ, Gorjón SP, Gunde-Cimerman N, Hyde KD, Kemler M, Li GJ, Liu DM, Liu XZ, Nuytinck J, Papp V, Savchenko A, Savchenko K, Tedersoo L, Theelen B, Thines M, Tomšovský M, Toome-Heller M, Urón JP, Verbeken A, Vizzini A, Yurkov AM, Zamora JC, Zhao RL (2021) Delimiting species in Basidiomycota: a review. Fungal Divers 109:181–237. 10.1007/s13225-021-00479-5

Carlson CJ, Hopkins S, Bell KC, Doña J, Godfrey SS, Kwak ML, Lafferty KD, Moir ML, Speer KA, Strona G, Torchin M, Wood CL. A global parasite conservation plan. Biol Cons. 2020;250:108596. doi: 10.1016/j.biocon.2020.108596. DOI

Cavara F. Di una nuova Laboulbeniacea Rickia wasmannii nov. gen. e nov. spec. Malpighia. 1899;13:173–188.

Cottrell TE, Riddick EW. Limited transmission of the ectoparasitic fungus Hesperomyces virescens between lady beetles. Psyche. 2012;2012:814378. doi: 10.1155/2012/814378. DOI

Crous PW, Osieck ER, Jurjević Ž, Boers J, van Iperen AL, Starink-Willemse M, Dima B, Balashov S, Bulgakov TS, Johnston PR, Morozova OV, Pinruan U, Sommai S, Alvarado P, Decock CA, Lebel T, McMullan-Fisher S, Moreno G, Shivas RG, Zhao L, Abdollahzadeh J, Abrinbana M, Ageev DV, Akhmetova G, Alexandrova AV, Altés A, Amaral AGG, Angelini C, Arenas F, Asselman P, Badali F, Baghela A, Bañares A, Barreto RW, Baseia IG, Bellanger JM, Berraf-Tebbal A, Biketova AYu, Bukharova NV, Burgess TI, Cabero J, Câmara MPS, Cano-Lira JF, Ceryngier P, Chávez R, Cowan D, de Lima AF, de L. Oliveira R, Denman S, Dang QN, dos Santos Vieira WA, Dovana F, Duarte IG, Eichmeier A, Erhard A, Esteve-Raventós F, Fellin A, Ferisin G, Ferreira RJ, Ferrer A, Finy P, Gaya E, Geering ADW, Gil-Durán C, Glässnerová K, Glushakova AM, Gramaje D, Guard FE, Guarnizo AL, Haelewaters D, Halling RE, Hill R, Hirooka Y, Hubka V, Iliushin VA, Ivanova DD, Ivanushkina NE, Jangsantear P, Justo A, Kachalkin AV, Kato S, Khamsuntorn P, Kirtsideli IY, Knapp DG, Kochkina GA, Koukol O, Kovács GM, Kruse J, Kumar TKA, Kušan I, Læssøe T, Larsson E, Lebel T, Lebeuf R, Levicán G, Loizides M, Lúcio PSM, Luangsa-ard JJ, Lukina EG, Magaña-Dueñas V, Maggs-Kölling G, Malysheva EF, Malysheva VF, Martín B, Martín MP, Matočec N, McTaggart AR, Mehrabi-Koushki M, Mešić A, Miller AN, Mironova P, Moreau PA, Morte A, Müller K, Nagy LG, Nanu S, Navarro-Ródenas A, Nel W, Nguyen TH, Nóbrega TF, Noordeloos ME, Olariaga I, Overton BE, Ozerskaya SM, Palani P, Pancorbo F, Papp V, Pawłowska J, Pham TQ, Phosri C, Pichai S, Popov ES, Portugal A, Pošta A, Reschke K, Reul M, Ricci GM, Rodríguez A, Romanowski J, Ruchikachorn N, Saar I, Safi A, Sakolrak B, Salzmann F, Sandoval-Denis M, Sangwichein E, Sanhueza L, Sato T, Sastoque A, Senn-Irlet B, Shibata A, Siepe K, Somrithipol S, Spetik M, Stchigel AM, Stuskova K, Suwannasai N, Tan YP, Thangavel R, Tiago I, Tiwari S, Tkalčec Z, Tomashevskaya MA, Tonegawa C, Tran HX, Tran NT, Trovão J, Trubitsyn VE, Van Wyk J, Vila J, Visagie CM, Vizzini A, Volobuev SV, Vu DT, Wangsawat N, Yaguchi T, Ferreira BW, de Souza AP, Vieira BS, Groenewald JZ. 2021. Fungal Planet description sheets: 1284–1382. Persoonia 47:178–374. 10.3767/persoonia.2021.47.06

De Kesel A. Relative importance of direct and indirect infection in the transmission of Laboulbenia slackensis (ascomycetes, Laboulbeniales) Belg J Bot. 1996;128(2):124–130.

De Kesel A. Host specificity and habitat preference of Laboulbenia slackensis. Mycologia. 1996;88(4):565–573. doi: 10.1080/00275514.1996.12026687. DOI

De Kesel A (1997) Contribution towards the study of the specificity of Laboulbeniales (Fungi, ascomycetes), with particular reference to the transmission, habitat preference and host-range of Laboulbenia slackensis. Ph.D. dissertation. University of Antwerp, Antwerp. 10.2307/3761150

De Kesel A. Identification and host-range of the genus Laboulbenia in Belgium. Sterbeeckia. 1998;18:13–31.

De Kesel A, Haelewaters D. Laboulbenia slackensis and L. littoralis sp. nov (Ascomycota, Laboulbeniales), two sibling species as a result of ecological speciation. Mycologia. 2014;106(3):407–414. doi: 10.3852/13-348. PubMed DOI

de Queiroz K. The general lineage concept of species, species criteria, and the process of speciation: a conceptual unification and terminological recommendations. In: Howard DJ, Berlocher SH, editors. Endless forms. Species and speciation. Oxford: Oxford University Press; 1998. pp. 57–75.

de Queiroz K. Species concepts and species delimitation. Syst Biol. 2007;56(6):879–886. doi: 10.1080/10635150701701083. PubMed DOI

Dobzhansky T. Complete reproductive isolation between two morphologically similar species of Drosophila. Ecology. 1946;27(3):205–211. doi: 10.2307/1932895. DOI

Ehrlich PR, Raven PA. Butterflies and plants: a study in coevolution. Evolution. 1964;18(4):586–608. doi: 10.1111/j.1558-5646.1964.tb01674.x. DOI

Furlong ST, Thibault KS, Morbelli LM, Quinn JJ, Rogers RA. Uptake and compartmentalization of fluorescent lipid analogs in larval Schistosoma mansoni. J Lipid Res. 1995;36(1):1–12. doi: 10.1016/S0022-2275(20)39749-2. PubMed DOI

Goldmann L, Weir A. Position specificity in Chitonomyces (Ascomycota, Laboulbeniomycetes) on Laccophilus (Coleoptera, Dytiscidae): a molecular approach resolves a century-old debate. Mycologia. 2012;104(5):1143–1158. doi: 10.3852/11-358. PubMed DOI

Goldmann L, Weir A. Molecular phylogeny of the Laboulbeniomycetes (Ascomycota) Fungal Biol. 2018;122(2–3):87–100. doi: 10.1016/j.funbio.2017.11.004. PubMed DOI

Goldmann L, Weir A, Rossi W. Molecular analysis reveals two new dimorphic species of Hesperomyces (Ascomycota, Laboulbeniomycetes) parasitic on the ladybird Coleomegilla maculata (Coleoptera, Coccinellidae) Fungal Biol. 2013;117(11–12):807–813. doi: 10.1016/j.funbio.2013.10.004. PubMed DOI

Grünig CR, Duo A, Sieber TN, Holdenrieder O. Assignment of species rank to six reproductively isolated cryptic species of the Phialocephala fortinii s.l.-Acephala applanata species complex. Mycologia. 2008;100(1):47–67. doi: 10.1080/15572536.2008.11832498. PubMed DOI

Gutierrez AC, Ordoqui E, Leclerque A, López Lastra C. A new species of Herpomyces (Laboulbeniomycetes: Herpomycetales) on Periplaneta fuliginosa (Blattodea: Blattidae) from Argentina. Mycologia. 2020;112(6):1184–1191. doi: 10.1080/00275514.2020.1726134. PubMed DOI

Haelewaters D, De Kesel A. Checklist of thallus-forming Laboulbeniomycetes from Belgium and the Netherlands, including Hesperomyces halyziae and Laboulbenia quarantenae spp. nov. MycoKeys. 2020;71:23–86. doi: 10.3897/mycokeys.71.53421. PubMed DOI PMC

Haelewaters D, Pfister DH (2019) Morphological species of Gloeandromyces (Ascomycota, Laboulbeniales) evaluated using single-locus species delimitation methods. Fungal Syst Evol 3:19–33. 10.3114/fuse.2019.03.03 PubMed PMC

Haelewaters D, Gorczak M, Pfliegler WP, Tartally A, Tischer M, Wrzosek M, Pfister DH. Bringing Laboulbeniales into the 21st century: enhanced techniques for extraction and PCR amplification of DNA from minute ectoparasitic fungi. IMA Fungus. 2015;6(2):363–372. doi: 10.5598/imafungus.2015.06.02.08. PubMed DOI PMC

Haelewaters D, De Kesel A, Pfister DH. Integrative taxonomy reveals hidden species within a common fungal parasite of ladybirds. Sci Rep. 2018;8(1):15966. doi: 10.1038/s41598-018-34319-5. PubMed DOI PMC

Haelewaters D, Boer P, Báthori F, Rádai Z, Reboleira ASP, Tartally A, Pfiegler W, De Kesel A, Nedvěd O. Studies of Laboulbeniales on Myrmica ants (IV): host-related diversity and thallus distribution patterns of Rickia wasmannii. Parasite. 2019;26:29. doi: 10.1051/parasite/2019028. PubMed DOI PMC

Haelewaters D, Pfliegler WP, Gorczak M, Pfister DH. Birth of an order: Comprehensive molecular phylogenetic study excludes Herpomyces (Fungi, Laboulbeniomycetes) from Laboulbeniales. Mol Phylogenet Evol. 2019;133:286–301. doi: 10.1016/j.ympev.2019.01.007. PubMed DOI

Haelewaters D, Zhao SY, De Kesel A, Handlin RE, Royer IR, Farrell BD, Pfister DH. Laboulbeniales (Ascomycota) of the Boston Harbor Islands II: species parasitizing Carabidae, and the Laboulbenia flagellata species complex. Northeast Nat. 2019;25(Special Issue 9):110–149. doi: 10.1656/045.025.s906. DOI

Haelewaters D, Gorczak M, Kaishian P, De Kesel A, Blackwell M. Laboulbeniomycetes, enigmatic fungi with a turbulent taxonomic history. In: Zaragoza Ó, editor. Encyclopedia of mycology. Oxford: Elsevier; 2021. pp. 263–283.

Haelewaters D, Schoutteten N, Medina-van Berkum P, Martin TE, Verbeken A, Aime MC. Pioneering a fungal inventory at Cusuco National Park. Honduras J Mesoamerican Biol. 2021;1(1):111–131.

Hawksworth DL, Rossman AY. Where are all the undescribed fungi? Phytopathology. 1997;87(9):888–891. doi: 10.1094/PHYTO.1997.87.9.888. PubMed DOI

Huldén L. Laboulbeniales (ascomycetes) of Finland and adjacent parts of the U.S.S.R. Karstenia. 1983;23:31–136. doi: 10.29203/ka.1983.221. DOI

Jacobs K, Holtzman K, Seifert KA. Phylogeny and biology of Gliocephalis hyalina, a biotrophic contact mycoparasite of Fusarium species. Mycologia. 2005;97(1):111–120. doi: 10.1080/15572536.2006.11832844. PubMed DOI

Keymer A, Gutjhar C. Cross-kingdom lipid transfer in arbuscular mycorrhiza symbiosis and beyond. Curr Opin Plant Biol. 2018;44:137–144. doi: 10.1016/j.pbi.2018.04.005. PubMed DOI

Kirschner R. Two new species of Pyxidiophora associated with bark beetles in Europe. Mycol Prog. 2003;2(3):209–218. doi: 10.1007/s11557-006-0058-z. DOI

Kloehn J, Blume M, Cobbold SA, Saunders EC, Dagley MJ, McConville MJ. Using metabolomics to dissect host–parasite interactions. Curr Opin Microbiol. 2016;32:59–65. doi: 10.1016/j.mib.2016.04.019. PubMed DOI

Konrad M, Grasse AV, Tragust S, Cremer S. Anti-pathogen protection versus survival costs mediated by an ectosymbiont in an ant host. Proc R Soc B. 2015;282(1799):20141976. doi: 10.1098/rspb.2014.1976. PubMed DOI PMC

Li YM, Shivas RG, Cai L. Cryptic diversity in Tranzscheliella spp. (Ustilaginales) is driven by host switches. Sci Rep. 2017;7(1):43549. doi: 10.1038/srep43549. PubMed DOI PMC

Lundqvist N. On the genus Pyxidiophora sensu lato (pyrenomycetes) Bot Notiser. 1980;133:121–144.

Maharachchikumbura SSN, Chen Y, Ariyawansa HA, Hyde KD, Haelewaters D, Perera RH, Samarakoon MC, Wanasinghe DN, Bustamante DE, Liu J-K, Lawrence DP, Cheewangkoon R, Stadler M (2021) Integrative approaches for species delimitation in Ascomycota. Fungal Divers 109:155–179. 10.1007/s13225-021-00486-6

Pfliegler WP, Báthori F, Haelewaters D, Tartally A. Studies of Laboulbeniales on Myrmica ants (III): myrmecophilous arthropods as alternative hosts of Rickia wasmannii. Parasite. 2016;23:50. doi: 10.1051/parasite/2016060. PubMed DOI PMC

Pringle A, Baker DM, Platt JL, Wares JP, Latge JP, Taylor JW. Cryptic speciation in the cosmopolitan and clonal human pathogenic fungus Aspergillus fumigatus. Evolution. 2005;59(9):1886–1899. doi: 10.1111/j.0014-3820.2005.tb01059.x. PubMed DOI

Reboleira ASP, Fresnada J, Salgado JM. A new species of Speonemadus from Portugal, with the revision of the escalerai-group (Coleoptera, Leiodidae) Eur J Taxon. 2017;261:1–23. doi: 10.5852/ejt.2017.261. DOI

Reboleira ASPS, Moritz L, Santamaria S, Enghofff H. Penetrative and non-penetrative interaction between Laboulbeniales fungi and their arthropod hosts. Sci Rep. 2021;11:22170. doi: 10.1038/s41598-021-01729-x. PubMed DOI PMC

Richards AG, Smith MN. Infection of cockroaches with Herpomyces (Laboulbeniales). III. Experimental studies on host specificity. Bot Gazette. 1954;116(2):195–198. doi: 10.1086/335861. DOI

Rossi W. New species of Laboulbenia from Ecuador, with evidence for host switch in the Laboulbeniales. Mycologia. 2011;103(1):184–194. doi: 10.3852/10-117. PubMed DOI

Santamaría S. Laboulbeniales, I. Laboulbenia. Flora Mycol. 1998;4:1–186.

Scheloske HW (1969) Beiträge zur Biologie, Ökologie und Systematik der Laboulbeniales (Ascomycetes) unter besondere Berücksichtigung des Parasit-Wirt-Verhältnisses. Parasitol Schriftenr 19:1–176

Scheloske HW. Eusynaptomyces benjaminii, spec. nova, (Ascomycetes, Laboulbeniales) und seinde Anpassungen an das Fortpflanzungsverhalten seines Wirtes Enochrus testaceus (Coleoptera, Hydrophilidae) Plant Syst Evolut. 1976;126(3):267–285. doi: 10.1007/BF00983366. DOI

Singh G, Dal Grande F, Divakar PK, Otte J, Leavitt SD, Szczepanska K, Crespo A, Rico VJ, Aptroot A, da Silva Cáceres ME, Lumbsch HT, Schmitt I. Coalescent-based species delimitation approach uncovers high cryptic diversity in the cosmopolitan lichen-forming fungal genus Protoparmelia (Lecanorales, Ascomycota) PLoS ONE. 2015;10(5):e0124625. doi: 10.1371/journal.pone.0124625. PubMed DOI PMC

Skrede I, Carlsen T, Schumacher T. A synopsis of the saddle fungi (Helvella: Ascomycota) in Europe–species delimitation, taxonomy and typification. Persoonia. 2017;39:201–253. doi: 10.3767/persoonia.2017.39.09. PubMed DOI PMC

Sochorová Z, Döbbeler P, Sochor M, van Rooy J. Octospora conidiophora (Pyronemataceae)—a new species from South Africa and the first report of anamorph in bryophilous Pezizales. MycoKeys. 2019;54:49–76. doi: 10.3897/mycokeys.54.34571. PubMed DOI PMC

Stanley DW, Nelson DR. Insect lipids: chemistry, biochemistry, and biology. Lincoln: University of Nebraska Press; 1993.

Stefani FO, Jones RH, May TW. Concordance of seven gene genealogies compared to phenotypic data reveals multiple cryptic species in Australian dermocyboid Cortinarius (Agaricales) Mol Phylogenet Evol. 2014;71:249–260. doi: 10.1016/j.ympev.2013.10.019. PubMed DOI

Sundberg H, Ekman S, Kruys Å. A crush on small fungi: an efficient and quick method for obtaining DNA from minute ascomycetes. Methods Ecol Evol. 2018;9(1):148–158. doi: 10.1111/2041-210X.12850. DOI

Sundberg H, Kruys Å, Bergsten J, Ekman S. Position specificity in the genus Coreomyces (Laboulbeniomycetes, Ascomycota) Fungal Syst Evolut. 2018;1:217–228. doi: 10.3114/fuse.2018.01.09. PubMed DOI PMC

Sundberg H, Kruys Å, Bergsten J, Ekman S. Coreomyces (Laboulbeniales) in Sweden, with two new species. Nord J Bot. 2021;39(11):e03323. doi: 10.1111/njb.03323. DOI

Tavares II. Laboulbeniales (Fungi, Ascomycetes) Mycol Mem. 1985;9:1–627.

Thaxter R (1896) Contribution towards a monograph of the Laboulbeniaceae. Mem Am Acad Arts Sci 12(3):187–429

Thaxter R (1931) Contribution towards a monograph of the Laboulbeniaceae. Part V. Mem Am Acad Arts Sci 16:1–435

Tragust S, Tartally A, Espadaler X, Billen J. Histopathology of Laboulbeniales (Ascomycota: Laboulbeniales): ectoparasitic fungi on ants (Hymenoptera: Formicidae) Myrmecol News. 2016;23:81–89.

Wang TW, de Kesel A, Haelewaters D, Pfister DH. Farlow Herbarium cockroach hosts new record of Laboulbeniales for North America. Rhodora. 2016;118(973):26–31. doi: 10.3119/15-20. DOI

Wang J, Guo X, Li L, Qiu H, Zhang Z, Wang Y, Sun G. Application of the fluorescent dye BODIPY in the study of lipid dynamics of the rice blast fungus Magnaporthe oryzae. Molecules. 2018;23(7):1594. doi: 10.3390/molecules23071594. PubMed DOI PMC

Weir A, Blackwell M. Extraction and PCR amplification of DNA from minute ectoparasitic fungi. Mycologia. 2001;93(4):802–806. doi: 10.2307/3761835. DOI

Weir A, Hammond PM. Laboulbeniales on beetles: host utilization patterns and species richness of the parasites. Biodivers Conserv. 1997;6(5):701–719. doi: 10.1023/A:1018318320019. DOI

Wenk MR. Lipidomics of host–pathogen interactions. FEBS Lett. 2006;580(23):5541–5551. doi: 10.1016/j.febslet.2006.07.007. PubMed DOI

Wijayawardene NN. The necessity of working with “orphaned” asexual genera. Ser Mycol Microbiol. 2019;1:1–3.

Yin M, Wingfield MJ, Zhou X, Linnakoski R, De Beer ZW. Taxonomy and phylogeny of the Leptographium olivaceum complex (Ophiostomatales, Ascomycota), including descriptions of six new species from China and Europe. MycoKeys. 2019;60:93–123. doi: 10.3897/mycokeys.60.39069. PubMed DOI PMC

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