Abstract
Endosymbiotic bacteria are commonly inhabitants of environmental isolates of Mucoromycota fungi. Described bacterial endosymbionts of Mucoromycota are related to Burkholderia and Mycoplasma lineages. Bacterial endosymbionts of Mucoromycota tend to be obligately dependent on their fungal host for nutrition, but bacterial endosymbionts are not always needed for normal vegetative growth by their fungal hosts. When present in the fungal cytosol, bacterial endosymbionts alter fungal physiology including gene expression, protein synthesis, metabolism, and sporulation. Many bacterial endosymbionts have steamlined genomes due to reductive evolution, and the categories of functional gene loss differ by fungal host lineage. Much remains to be learned about bacterial endosymbionts of fungi regarding their ubiquity, transmission, and fungal host interactions.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Bennett GM, Moran NA (2013) Small, smaller, smallest: the origins and evolution of ancient dual symbioses in a phloem-feeding insect. Genome Biol Evol 5(9):1675–1688. https://doi.org/10.1093/gbe/evt118
Bertaux J, Schmid M, Prevost-Boure NC, Churin JL, Hartmann A, Garbaye J, Frey-Klett P (2003) In situ identification of intracellular bacteria related to Paenibacillus spp. in the mycelium of the ectomycorrhizal fungus Laccaria bicolor S238N. Appl Environ Microbiol 69(7):4243–4248. https://doi.org/10.1128/aem.69.7.4243-4248.2003
Bianciotto V, Bandi C, Minerdi DANIELA, Sironi M, Volker H, Titchy A, Bonfante P (1996) An obligately endosymbiotic mycorrhizal fungus itself harbors obligately intracellular bacteria. Appl Environ Microbiol 62(8):3005–3010
Bianciotto V, Lumini E, Bonfante P, Vandamme P (2003) ‘Candidatus Glomeribacter gigasporarum’gen. Nov., sp. nov., an endosymbiont of arbuscular mycorrhizal fungi. Int J Syst Evol Microbiol 53(1):121–124
Bonfante P, Desirò A (2017) Who lives in a fungus? The diversity, origins and functions of fungal endobacteria living in Mucoromycota. ISME J 11(8):1727–1735
Bonfante P, Balestrini R, Mend Gen K (1994) Storage and secretion processes in the spore of Gigaspora margarita Becker &Hall as revealed by high-pressure freezing and freeze substitution. New Phytol 128(1):93–101
Brendel N, Partida-Martinez LP, Scherlach K, Hertweck C (2007) A cryptic PKS–NRPS gene locus in the plant commensal Pseudomonas fluorescens pf-5 codes for the biosynthesis of an antimitotic rhizoxin complex. Org Biomol Chem 5(14):2211–2213
Brundrett MC, Tedersoo L (2018) Evolutionary history of mycorrhizal symbioses and global host plant diversity. New Phytol 220(4):1108–1115
Büttner H, Niehs SP, Vandelannoote K, Cseresnyés Z, Dose B, Richter I, Gerst R, Figge MT, Stinear TP, Pidot SJ (2021) Bacterial endosymbionts protect beneficial soil fungus from nematode attack. Proc Natl Acad Sci 118(37):e2110669118
Cabrera-Rangel JF, Mendoza-Servın JV, Cordova-Lopez G, Alcalde-Vazquez R, Garcıa-Estrada RS, Winkler R, Partida-Martınez LP (2022) Symbiotic and toxinogenic Rhizopus spp. isolated from soils of different papaya producing regions in Mexico
Carter ME, Carpenter SC, Dubrow ZE, Sabol MR, Rinaldi FC, Lastovetsky OA, Mondo SJ, Pawlowska TE, Bogdanove AJ (2020) A TAL effector-like protein of an endofungal bacterium increases the stress tolerance and alters the transcriptome of the host. Proc Natl Acad Sci 117(29):17122–17129
Chang Y, Wang S, Sekimoto S, Aerts AL, Choi C, Clum A, LaButti KM, Lindquist EA, Yee Ngan C, Ohm RA (2015a) Phylogenomic analyses indicate that early fungi evolved digesting cell walls of algal ancestors of land plants. Genome Biol Evol 7(6):1590–1601
Chang Y, Wang S, Sekimoto S, Aerts AL, Choi C, Clum A, LaButti KM, Lindquist EA, Ngan CY, Ohm RA (2015b) Phylogenomic analyses indicate that early fungi evolved digesting cell walls of algal ancestors of land plants. Genome Biol Evol 7(6):1590–1601
Chang Y, Desirò A, Na H, Sandor L, Lipzen A, Clum A, Barry K, Grigoriev IV, Martin FM, Stajich JE (2019) Phylogenomics of Endogonaceae and evolution of mycorrhizas within Mucoromycota. New Phytol 222(1):511–525
Cheng C, Hua ZC (2020) Lasso peptides: heterologous production and potential medical application. Front Bioeng Biotechnol 8:571165. https://doi.org/10.3389/fbioe.2020.571165
Cruz-Lachica I, Márquez-Zequera I, García-Estrada RS, Carrillo-Fasio JA, León-Félix J, Allende-Molar R (2017) Identification of mucoralean fungi causing soft rot in papaya (Carica papaya L.) fruit in Mexico. Revista mexicana de fitopatología 35(3):397–417
Dearth SP, Castro HF, Venice F, Tague ED, Novero M, Bonfante P, Campagna SR (2018) Metabolome changes are induced in the arbuscular mycorrhizal fungus Gigaspora margarita by germination and by its bacterial endosymbiont. Mycorrhiza 28(5):421–433
Desirò A, Naumann M, Epis S, Novero M, Bandi C, Genre A, Bonfante P (2013) Mollicutes-related endobacteria thrive inside liverwort-associated arbuscular mycorrhizal fungi. Environ Microbiol 15(3):822–836. https://doi.org/10.1111/j.1462-2920.2012.02833.x
Desirò A, Salvioli A, Ngonkeu EL, Mondo SJ, Epis S, Faccio A, Kaech A, Pawlowska TE, Bonfante P (2014) Detection of a novel intracellular microbiome hosted in arbuscular mycorrhizal fungi. ISME J 8(2):257–270
Desirò A, Faccio A, Kaech A, Bidartondo MI, Bonfante P (2015a) Endogone, one of the oldest plant-associated fungi, host unique Mollicutes-related endobacteria. New Phytol 205(4):1464–1472
Desirò A, Salvioli A, Bonfante P (2015b) Investigating the Endobacteria which thrive in arbuscular mycorrhizal fungi. Methods Mol Biol (Clifton, NJ) 1399:29–53
Desirò A, Rimington WR, Jacob A, Pol NV, Smith ME, Trappe JM, Bidartondo MI, Bonito G (2017) Multigene phylogeny of Endogonales, an early diverging lineage offungi associated with plants. IMA Fungus 8(2):245–257
Desirò A, Hao Z, Liber JA, Benucci GMN, Lowry D, Roberson R, Bonito G (2018) Mycoplasma-related endobacteria within Mortierellomycotina fungi: diversity, distribution and functional insights into their lifestyle. ISME J 12(7):1743
Deveau A, Bonito G, Uehling J, Paoletti M, Becker M, Bindschedler S, Hacquard S, Hervé V, Labbé J, Lastovetsky O (2018) Bacterial-fungal interactions: ecology, mechanisms and challenges. FEMS Microbiol Rev 42(3):335–352
Dixon-Stewart D (1932) Species of Mortierella isolated from soil. Trans Br Mycol Soc 17(3):208–220
Dolatabadi S, Scherlach K, Figge M, Hertweck C, Dijksterhuis J, Menken SB, de Hoog GS (2016) Food preparation with mucoralean fungi: a potential biosafety issue? Fungal Biol 120(3):393–401
Espino-Vázquez AN, Bermúdez-Barrientos JR, Cabrera-Rangel J, Córdova-López G, Cardoso-Martínez F, Martínez-Vázquez A, Camarena-Pozos DA, Mondo SJ, Pawlowska TE, Abreu-Goodger C (2020) Narnaviruses: novel players in fungal–bacterial symbioses. ISME J 14(7):1743–1754
Estrada-de Los Santos P, Palmer M, Chávez-Ramírez B, Beukes C, Steenkamp ET, Briscoe L, Khan N, Maluk M, Lafos M, Humm E (2018) Whole genome analyses suggests that Burkholderia sensu lato contains two additional novel genera (Mycetohabitans gen. Nov., and Trinickia gen. Nov.): implications for the evolution of diazotrophy and nodulation in the Burkholderiaceae. Genes 9(8):389
Field KJ, Rimington WR, Bidartondo MI, Allinson KE, Beerling DJ, Cameron DD, Duckett JG, Leake JR, Pressel S (2015) First evidence of mutualism between ancient plant lineages (H aplomitriopsida liverworts) and M ucoromycotina fungi and its response to simulated P alaeozoic changes in atmospheric CO 2. New Phytol 205(2):743–756
Frey-Klett P, Burlinson P, Deveau A, Barret M, Tarkka M, Sarniguet A (2011) Bacterial-fungal interactions: hyphens between agricultural, clinical, environmental, and food microbiologists. Microbiol Mol Biol Rev 75(4):583–609. https://doi.org/10.1128/MMBR.00020-11
Fujimura R, Nishimura A, Ohshima S, Sato Y, Nishizawa T, Oshima K, Hattori M, Narisawa K, Ohta H (2014) Draft genome sequence of the Betaproteobacterial endosymbiont associated with the fungus Mortierella elongata FMR23-6. Genome Announc 2(6):e01272-14. https://doi.org/10.1128/genomeA.01272-14
Gams W (1977) A key to the species of Mortierella. Persoonia 9(3):381–391
Genre A, Lanfranco L, Perotto S, Bonfante P (2020) Unique and common traits in mycorrhizal symbioses. Nat Rev Microbiol 18(11):649–660
Ghignone S, Salvioli A, Anca I, Lumini E, Ortu G, Petiti L, Cruveiller S, Bianciotto V, Piffanelli P, Lanfranco L, Bonfante P (2012) The genome of the obligate endobacterium of an AM fungus reveals an interphylum network of nutritional interactions. ISME J 6(1):136–145. https://doi.org/10.1038/ismej.2011.110
Gho N, Yaoita T, Aoyagi K, Sato Z (1978) Studies on the control of Rhizopus in the nursery cases of rice seedlings, 5: influence of a phytotoxic substance produced by Rhizopus in growth of rice. In: Proceedings of the Association for Plant Protection of Hokuriku
Glaeser SP, Imani J, Alabid I, Guo H, Kumar N, Kämpfer P, Hardt M, Blom J, Goesmann A, Rothballer M (2015) Non-pathogenic rhizobium radiobacter F4 deploys plant beneficial activity independent of its host Piriformospora indica. ISME J 10(4):871–884
Gnanesh B, Tejaswi A, Arunakumar G, Supriya M, Manojkumar H, Tewary P (2021) Molecular phylogeny, identification and pathogenicity of Rhizopus oryzae associated with root rot of mulberry in India. J Appl Microbiol 131(1):360–374
Goyzueta-Mamani L, de Carvalho J, Magalhães A Jr, Soccol C (2021) Production of arachidonic acid by Mortierella alpina using wastes from potato chips industry. J Appl Microbiol 130(5):1592–1601
Guo Y, Takashima Y, Sato Y, Narisawa K, Ohta H, Nishizawa T (2020) Mycoavidus sp. strain B2-EB: comparative genomics reveals minimal genomic features required by a cultivable Burkholderiaceae-related endofungal bacterium. Appl Environ Microbiol 86(18):e01018–e01020
Herlambang A, Guo Y, Takashima Y, Narisawa K, Ohta H, Nishizawa T (2022) Whole-genome sequence of Entomortierella parvispora E1425, a Mucoromycotan fungus associated with Burkholderiaceae-related endosymbiotic bacteria. Microbiol Resour Announc 11(1):e01101–e01121
Hibbett DS, Binder M, Bischoff JF, Blackwell M, Cannon PF, Eriksson OE, Huhndorf S, James T, Kirk PM, Lücking R (2007) A higher-level phylogenetic classification of the fungi. Mycol Res 111(5):509–547
Hirose D, Degawa Y, Inaba S, Tokumasu S (2012) The anamorphic genus Calcarisporiella is a new member of the Mucoromycotina. Mycoscience 53(4):256–260
Hirose D, Degawa Y, Yamamoto K, Yamada A (2014) Sphaerocreas pubescens is a member of the Mucoromycotina closely related to fungi associated with liverworts and hornworts. Mycoscience 55(3):221–226
Hoffman MT, Arnold AE (2010) Diverse bacteria inhabit living hyphae of phylogenetically diverse fungal endophytes. Appl Environ Microbiol 76(12):4063–4075. https://doi.org/10.1128/AEM.02928-09
Horn F, Üzüm Z, Möbius N, Guthke R, Linde J, Hertweck C (2015) Draft genome sequences of symbiotic and nonsymbiotic Rhizopus microsporus strains CBS 344.29 and ATCC 62417. Genome Announc 3(1):e01370–e01314. https://doi.org/10.1128/genomeA.01370-14
Ibrahim AS, Gebremariam T, Liu M, Chamilos G, Kontoyiannis DP, Mink R, Kwon-Chung KJ, Fu Y, Skory CD, Edwards JE Jr (2008) Bacterial endosymbiosis is widely present among zygomycetes but does not contribute to the pathogenesis of mucormycosis. J Infect Dis 198(7):1083–1090
Itabangi H, Sephton-Clark PC, Tamayo DP, Zhou X, Starling GP, Mahamoud Z, Insua I, Probert M, Correia J, Moynihan PJ (2022) A bacterial endosymbiont of the fungus Rhizopus microsporus drives phagocyte evasion and opportunistic virulence. Current biology 32(5):1115–1130. e1116
Iwasaki S, Kobayashi H, Furukawa J, Namikoshi M, Okuda S, Sato Z, Matsuda I, Noda T (1984) Studies on macrocyclic lactone antibiotics. vii structure of a phytotoxin. J Antibiot 37(4):354–362
James TY, Kauff F, Schoch CL, Matheny PB, Hofstetter V, Cox CJ, Celio G, Gueidan C, Fraker E, Miadlikowska J, Lumbsch HT, Rauhut A, Reeb V, Arnold AE, Amtoft A, Stajich JE, Hosaka K, Sung GH, Johnson D, O’Rourke B, Crockett M, Binder M, Curtis JM, Slot JC, Wang Z, Wilson AW, Schussler A, Longcore JE, O’Donnell K, Mozley-Standridge S, Porter D, Letcher PM, Powell MJ, Taylor JW, White MM, Griffith GW, Davies DR, Humber RA, Morton JB, Sugiyama J, Rossman AY, Rogers JD, Pfister DH, Hewitt D, Hansen K, Hambleton S, Shoemaker RA, Kohlmeyer J, Volkmann-Kohlmeyer B, Spotts RA, Serdani M, Crous PW, Hughes KW, Matsuura K, Langer E, Langer G, Untereiner WA, Lucking R, Budel B, Geiser DM, Aptroot A, Diederich P, Schmitt I, Schultz M, Yahr R, Hibbett DS, Lutzoni F, McLaughlin DJ, Spatafora JW, Vilgalys R (2006) Reconstructing the early evolution of fungi using a six-gene phylogeny. Nature 443(7113):818–822. https://doi.org/10.1038/nature05110
Jargeat P, Cosseau C, Ola’h B, Jauneau A, Bonfante P, Batut J, Becard G (2004) Isolation, free-living capacities, and genome structure of “Candidatus Glomeribacter gigasporarum,” the endocellular bacterium of the mycorrhizal fungus Gigaspora margarita. J Bacteriol 186(20):6876–6884
Jeon KW (1972) Development of cellular dependence on infective organisms: micrurgical studies in amoebas. Science 176(4039):1122–1123
Jeong W, Keighley C, Wolfe R, Lee WL, Slavin M, Kong D, Chen S-A (2019) The epidemiology and clinical manifestations of mucormycosis: a systematic review and meta-analysis of case reports. Clin Microbiol Infect 25(1):26–34
Koczyk G, Pawłowska J, Muszewska A (2021) Terpenoid biosynthesis dominates among secondary metabolite clusters in mucoromycotina genomes. J Fungi 7(4):285
Kondo H, Botella L, Suzuki N (2022) Mycovirus diversity and evolution revealed/inferred from recent studies. Annu Rev Phytopathol 60:307–336
Kuga Y, Wu T-D, Sakamoto N, Katsuyama C, Yurimoto H (2021) Allocation of carbon from an arbuscular mycorrhizal fungus, Gigaspora margarita, to its gram-negative and positive Endobacteria revealed by high-resolution secondary ion mass spectrometry. Microorganisms 9(12):2597
Lackner G, Hertweck C (2011) Impact of endofungal bacteria on infection biology, food safety, and drug development. PLoS Pathog 7(6):e1002096
Lackner G, Partida-Martinez LP, Hertweck C (2009) Endofungal bacteria as producers of mycotoxins. Trends Microbiol 17(12):570–576. https://doi.org/10.1016/j.tim.2009.09.003
Lackner G, Moebius N, Hertweck C (2011a) Endofungal bacterium controls its host by an hrp type III secretion system. ISME J 5(2):252–261. https://doi.org/10.1038/ismej.2010.126
Lackner G, Moebius N, Partida-Martinez LP, Boland S, Hertweck C (2011b) Evolution of an endofungal lifestyle: deductions from the Burkholderia rhizoxinica genome. BMC Genomics 12(1):1–13
Lackner G, Moebius N, Partida-Martinez L, Hertweck C (2011c) Complete genome sequence of Burkholderia rhizoxinica, an endosymbiont of Rhizopus microsporus. J Bacteriol 193(3):783–784
Lastovetsky OA, Gaspar ML, Mondo SJ, LaButti KM, Sandor L, Grigoriev IV, Henry SA, Pawlowska TE (2016) Lipid metabolic changes in an early divergent fungus govern the establishment of a mutualistic symbiosis with endobacteria. Proc Natl Acad Sci 113(52):201615148
Lastovetsky OA, Ahn E, Mondo SJ, Toomer KH, Zhang A, Johnson LM, Pawlowska TE (2018) Distribution and population structure of endobacteria in arbuscular mycorrhizal fungi at North Atlantic dunes. ISME J 12(12):3001–3013
Leone MR, Lackner G, Silipo A, Lanzetta R, Molinaro A, Hertweck C (2010) An unusual galactofuranose lipopolysaccharide that ensures the intracellular survival of toxin-producing bacteria in their fungal host. Angew Chem Int Ed 49(41):7476–7480
Li Z, Yao Q, Dearth SP, Entler MR, Castro Gonzalez HF, Uehling JK, Vilgalys RJ, Hurst GB, Campagna SR, Labbé JL (2017) Integrated proteomics and metabolomics suggests symbiotic metabolism and multimodal regulation in a fungal-endobacterial system. Environ Microbiol 19(3):1041–1053
Liao H-L (2021) The plant-growth-promoting fungus, Mortierella elongata: its biology, ecological distribution, and growth-promoting activities: SS679/SL466, 3/2021. EDIS 2021(2)
Liao H-L, Bonito G, Rojas JA, Hameed K, Wu S, Schadt CW, Labbé J, Tuskan GA, Martin F, Grigoriev IV (2019) Fungal endophytes of Populus trichocarpa alter host phenotype, gene expression, and rhizobiome composition. Mol Plant-Microbe Interact 32(7):853–864
Liu Y, Steenkamp ET, Brinkmann H, Forget L, Philippe H, Lang BF (2009) Phylogenomic analyses predict sistergroup relationship of nucleariids and fungi and paraphyly of zygomycetes with significant support. BMC Evol Biol 9(1):1–11
Lumini E, Bianciotto V, Jargeat P, Novero M, Salvioli A, Faccio A, Becard G, Bonfante P (2007) Presymbiotic growth and sporal morphology are affected in the arbuscular mycorrhizal fungus Gigaspora margarita cured of its endobacteria. Cell Microbiol 9(7):1716–1729. https://doi.org/10.1111/j.1462-5822.2007.00907.x
MacDonald R, Chandler MR (1981) Bacterium-like organelles in the vesicular-arbuscular mycorrhizal fungus Glomus caledonius. New Phytol 89(2):241–246
Macias AM, Marek PE, Morrissey EM, Brewer MS, Short DP, Stauder CM, Wickert KL, Berger MC, Metheny AM, Stajich JE (2019) Diversity and function of fungi associated with the fungivorous millipede, Brachycybe lecontii. Fungal Ecol 41:187–197
Mamani LDG, Magalhães AI Jr, Ruan Z, de Carvalho JC, Soccol CR (2019) Industrial production, patent landscape, and market trends of arachidonic acid-rich oil of Mortierella alpina. Biotechnol Res Innov 3(1):103–119
Meyer W, Walter G (2003) Delimitation of Umbelopsis (Mucorales, Umbelopsidaceae fam. Nov.) based on ITS sequence and RFLP data. Mycol Res 107(3):339–350
Moebius N, Üzüm Z, Dijksterhuis J, Lackner G, Hertweck C (2014) Active invasion of bacteria into living fungal cells. elife 3:e03007
Mondo SJ, Toomer KH, Morton JB, Lekberg Y, Pawlowska TE (2012) Evolutionary stability in a 400-million-year-old heritable facultative mutualism. Evolution 66(8):2564–2576
Mondo SJ, Salvioli A, Bonfante P, Morton JB, Pawlowska TE (2016) Nondegenerative evolution in ancient heritable bacterial endosymbionts of fungi. Mol Biol Evol 33(9):msw086
Mondo SJ, Lastovetsky OA, Gaspar ML, Schwardt NH, Barber CC, Riley R, Sun H, Grigoriev IV, Pawlowska TE (2017) Bacterial endosymbionts influence host sexuality and reveal reproductive genes of early divergent fungi. Nat Commun 8(1):1843
Moreau F (1952) Les champignons, physiologie, morphologie développement ét systematique
Mosse B (1962) The establishment of vesicular-arbuscular mycorrhiza under aseptic conditions. Microbiology 27(3):509–520
Mosse B (1970) Honey-coloured, sessile Endogone spores: II. Changes in fine structure during spore development. Arch Mikrobiol 74(2):129–145
Mullins AJ, Mahenthiralingam E (2021) The hidden genomic diversity, specialized metabolite capacity, and revised taxonomy of Burkholderia sensu lato. Front Microbiol 12:726847
Myers J (2020) The diversity of Mycoviruses in early-diverging fungi, and their evolutionary implications (Doctoral dissertation)
Myers J, Bonds A, Clemons R, Thapa N, Simmons D, Carter-House D, Ortanez J, Liu P, Miralles-Durán A, Desirò A (2020) Survey of early-diverging lineages of fungi reveals abundant and diverse mycoviruses. MBio 11(5):e02027–e02020
Naito M, Pawlowska TE (2016) Defying Muller’s ratchet: ancient heritable endobacteria escape extinction through retention of recombination and genome plasticity. MBio 7(3):e02057–e02015
Naito M, Morton JB, Pawlowska TE (2015) Minimal genomes of mycoplasma-related endobacteria are plastic and contain host-derived genes for sustained life within Glomeromycota. Proc Natl Acad Sci U S A 112(25):7791–7796. https://doi.org/10.1073/pnas.1501676112
Naito M, Desirò A, González JB, Tao G, Morton JB, Bonfante P, Pawlowska TE (2017) ‘Candidatus Moeniiplasma glomeromycotorum’, an endobacterium of arbuscular mycorrhizal fungi. Int J Syst Evol Microbiol 67(5):1177–1184
Naumann M, Schussler A, Bonfante P (2010) The obligate endobacteria of arbuscular mycorrhizal fungi are ancient heritable components related to the Mollicutes. ISME J 4(7):862–871. https://doi.org/10.1038/ismej.2010.21
Niehs SP, Scherlach K, Hertweck C (2018a) Genomics-driven discovery of a linear lipopeptide promoting host colonization by endofungal bacteria. Org Biomol Chem 16(37):8345–8352. https://doi.org/10.1039/C8OB01515E
Niehs SP, Dose B, Scherlach K, Roth M, Hertweck C (2018b) Genomics-driven discovery of a symbiont-specific cyclopeptide from bacteria residing in the rice seedling blight fungus. Chembiochem 19(20):2167–2172. https://doi.org/10.1002/cbic.201800400
Niehs SP, Dose B, Scherlach K, Pidot SJ, Stinear TP, Hertweck C (2019) Genome mining reveals endopyrroles from a nonribosomal peptide assembly line triggered in fungal–bacterial symbiosis. ACS Chem Biol 14(8):1811–1818. https://doi.org/10.1021/acschembio.9b00406
Niehs SP, Dose B, Richter S, Pidot SJ, Dahse HM, Stinear TP, Hertweck C (2020) Mining symbionts of a spider-transmitted fungus illuminates uncharted biosynthetic pathways to cytotoxic benzolactones. Angew Chem Int Ed 59(20):7766–7771. https://doi.org/10.1002/anie.201916007
Niehs SP, Scherlach K, Dose B, Uzum Z, Stinear TP, Pidot SJ, Hertweck C (2022) A highly conserved gene locus in endofungal bacteria codes for the biosynthesis of symbiosis-specific cyclopeptides. PNAS Nexus 1(4):pgac152
Ohshima S, Sato Y, Fujimura R, Takashima Y, Hamada M, Nishizawa T, Narisawa K, Ohta H (2016) Mycoavidus cysteinexigens gen. Nov., sp. nov., an endohyphal bacterium isolated from a soil isolate of the fungus Mortierella elongata. Int J Syst Evol Microbiol 66(5):2052–2057
Ohta T (1972) Population size and rate of evolution. J Mol Evol 1(4):305–314
Okrasińska A, Bokus A, Duk K, Gęsiorska A, Sokołowska B, Miłobędzka A, Wrzosek M, Pawłowska J (2021) New endohyphal relationships between mucoromycota and burkholderiaceae representatives. Appl Environ Microbiol 87(7):e02707–e02720
Papanikolaou S, Aggelis G (2019) Sources of microbial oils with emphasis to Mortierella (Umbelopsis) isabellina fungus. World J Microbiol Biotechnol 35(4):1–19
Partida-Martinez LP (2013) A model for bacterial-fungal interactions. LAP LAMBERT Academic Publishing, London
Partida-Martinez LP, Hertweck C (2005) Pathogenic fungus harbours endosymbiotic bacteria for toxin production. Nature 437(7060):884–888. https://doi.org/10.1038/nature03997
Partida-Martinez LP, Hertweck C (2007) A gene cluster encoding rhizoxin biosynthesis in “Burkholderia rhizoxina”, the bacterial endosymbiont of the fungus Rhizopus microsporus. Chembiochem 8(1):41–45. https://doi.org/10.1002/cbic.200600393
Partida-Martinez LP, Monajembashi S, Greulich KO, Hertweck C (2007) Endosymbiont-dependent host reproduction maintains bacterial-fungal mutualism. Curr Biol 17(9):773–777. https://doi.org/10.1016/j.cub.2007.03.039. Epub 2007 Apr 5. PMID: 17412585
Partida-Martínez LP (2017) The fungal holobiont: evidence from early diverging fungi. Environ Microbiol 19(8):2919–2923. https://doi.org/10.1111/1462-2920.13731. Epub 2017 Apr 3. PMID: 28295957
Pawlowska TE, Gaspar ML, Lastovetsky OA, Mondo SJ, Real-Ramirez I, Shakya E, Bonfante P (2018) Biology of fungi and their bacterial endosymbionts. Annu Rev Phytopathol 56(1):289–309
Petrikkos G, Skiada A, Lortholary O, Roilides E, Walsh TJ, Kontoyiannis DP (2012) Epidemiology and clinical manifestations of mucormycosis. Clin Infect Dis 54(suppl_1):S23–S34
Petrikkos G, Skiada A, Drogari-Apiranthitou M (2014) Epidemiology of mucormycosis in Europe. Clin Microbiol Infect 20:67–73
Redecker D, Kodner R, Graham LE (2000) Glomalean fungi from the Ordovician. Science 289(5486):1920–1921
Remy W, Taylor TN, Hass H, Kerp H (1994) Four hundred-million-year-old vesicular arbuscular mycorrhizae. Proc Natl Acad Sci 91(25):11841–11843
Richter I, Uzum Z, Stanley CE, Moebius N, Stinear TP, Pidot SJ, Ferling I, Hillmann F, Hertweck C (2020) Secreted TAL effectors protect symbiotic bacteria from entrapment within fungal hyphae. bioRxiv:2020–03. https://doi.org/10.1101/2020.03.28.013177
Richter I, Radosa S, Cseresnyés Z, Ferling I, Büttner H, Niehs SP, Gerst R, Scherlach K, Figge MT, Hillmann F (2022) Toxin-producing endosymbionts shield pathogenic fungus against micropredators. MBio 13(5):e01440–e01422
Robinson AJ, House GL, Morales DP, Kelliher JM, Gallegos-Graves LV, LeBrun ES, Davenport KW, Palmieri F, Lohberger A, Bregnard D (2021) Widespread bacterial diversity within the bacteriome of fungi. Commun Biol 4(1):1–13
Ropars J, Toro KS, Noel J, Pelin A, Charron P, Farinelli L, Marton T, Krüger M, Fuchs J, Brachmann A (2016) Evidence for the sexual origin of heterokaryosis in arbuscular mycorrhizal fungi. Nat Microbiol 1(6):1–9
Roux S, Krupovic M, Daly RA, Borges AL, Nayfach S, Schulz F, Sharrar A, Matheus Carnevali PB, Cheng J-F, Ivanova NN (2019) Cryptic inoviruses revealed as pervasive in bacteria and archaea across Earth’s biomes. Nat Microbiol 4(11):1895–1906
Salvioli di Fossalunga A, Lipuma J, Venice F, Dupont L, Bonfante P (2017) The endobacterium of an arbuscular mycorrhizal fungus modulates the expression of its toxin–antitoxin systems during the life cycle of its host. ISME J 11(10):2394–2398
Salvioli A, Lumini E, Anca IA, Bianciotto V, Bonfante P (2008) Simultaneous detection and quantification of the unculturable microbe Candidatus Glomeribacter gigasporarum inside its fungal host Gigaspora margarita. New Phytol 180(1):248–257
Salvioli A, Chiapello M, Fontaine J, Hadj-Sahraoui AL, Grandmougin-Ferjani A, Lanfranco L, Bonfante P (2010) Endobacteria affect the metabolic profile of their host Gigaspora margarita, an arbuscular mycorrhizal fungus. Environ Microbiol 12(8):2083–2095
Salvioli A, Ghignone S, Novero M, Navazio L, Bagnaresi P, Bonfante P (2016) Symbiosis with an endobacterium increases the fitness of a mycorrhizal fungus, raising its bioenergetic potential. ISME J 10(1):130–144
Sato Y, Narisawa K, Tsuruta K, Umezu M, Nishizawa T, Tanaka K, Yamaguchi K, Komatsuzaki M, Ohta H (2010) Detection of Betaproteobacteria inside the mycelium of the fungus Mortierella elongata. Microbes Environ 25(4):321–324. https://doi.org/10.1264/jsme2.ME10134
Scannerini S, Bonfante P 1975 Fontana a ultrastructural model for the host-symbiont interaction in the endotrophic mycorrhizae of Ornithogalum umbellatum L. In: Endomycorrhizas; Proceedings of a Symposium
Scannerini S, Bonfante P (1991) Bacteria and bacteria like objects in endomycorrhizal fungi (Glomaceae). Symbiosis as Source of Evolutionary Innovation: Speciation and Morphogenesis:273–287
Scherlach K, Partida-Martinez LP, Dahse H-M, Hertweck C (2006) Antimitotic Rhizoxin derivatives from a cultured bacterial endosymbiont of the Rice pathogenic fungus Rhizopus m icrosporus. J Am Chem Soc 128(35):11529–11536
Scherlach K, Busch B, Lackner G, Paszkowski U, Hertweck C (2012) Symbiotic cooperation in the biosynthesis of a phytotoxin. Angew Chem Int Ed 51(38):9615–9618. https://doi.org/10.1002/anie.201204540
Schüßler A, Mollenhauer D, Schnepf E, Kluge M (1994) Geosiphon pyriforme, an endosymbiotic association of fungus and cyanobacteria: the spore structure resembles that of arbuscular mycorrhizal (AM) fungi. Botanica Acta 107(1):36–45
Schüßler A, Bonfante P, Schnepf E et al (1996) Characterization of the Geosiphon pyriforme symbiosome by affinity techniques: confocal laser scanning microscopy (CLSM) and electron microscopy. Protoplasma 190:53–67. https://doi.org/10.1007/BF01281194
Sharmin D, Guo Y, Nishizawa T, Ohshima S, Sato Y, Takashima Y, Narisawa K, Ohta H (2018) Comparative genomic insights into endofungal lifestyles of two bacterial endosymbionts, Mycoavidus cysteinexigens and Burkholderia rhizoxinica. Microbe Environ 33(1):17138
Smith SE, Read DJ (2010) Mycorrhizal symbiosis. Academic press
Smith ME, Gryganskyi A, Bonito G, Nouhra E, Moreno-Arroyo B, Benny G (2013) Phylogenetic analysis of the genus Modicella reveals an independent evolutionary origin of sporocarp-forming fungi in the Mortierellales. Fungal Genet Biol 61:61–68
Spatafora JW, Chang Y, Benny GL, Lazarus K, Smith ME, Berbee ML, Bonito G, Corradi N, Grigoriev I, Gryganskyi A (2016) A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data. Mycologia 108(5):1028–1046
Sun X, Chen W, Ivanov S, MacLean AM, Wight H, Ramaraj T, Mudge J, Harrison MJ, Fei Z (2019) Genome and evolution of the arbuscular mycorrhizal fungus Diversispora epigaea (formerly glomus versiforme) and its bacterial endosymbionts. New Phytol 221(3):1556–1573
Sward R (1981) The structure of the spores of Gigaspora margaritaI The dormant spore. New Phytol 87(4):761–768
Szabó G, Schulz F, Manzano-Marín A, Toenshoff ER, Horn M (2022) Evolutionarily recent dual obligatory symbiosis among adelgids indicates a transition between fungus-and insect-associated lifestyles. ISME J 16(1):247–256
Tabima JF, Trautman IA, Chang Y, Wang Y, Mondo S, Kuo A, Salamov A, Grigoriev IV, Stajich JE, Spatafora JW (2020) Phylogenomic analyses of non-Dikarya fungi supports horizontal gene transfer driving diversification of secondary metabolism in the amphibian gastrointestinal symbiont, Basidiobolus. G3: genes, genomes, Genetics 10(9):3417–3433
Takashima Y, Degawa Y, Ohta H, Narisawa K (2018a) Mortierella sugadairana, a new homothallic species related to the firstly described heterothallic species in the genus. Mycoscience 59(3):200–205
Takashima Y, Seto K, Degawa Y, Guo Y, Nishizawa T, Ohta H, Narisawa K (2018b) Prevalence and intra-family phylogenetic divergence of Burkholderiaceae-related endobacteria associated with species of Mortierella. Microbe Environ 33(4):18081
Takashima Y, Degawa Y, Nishizawa T, Ohta H, Narisawa K (2020) Aposymbiosis of a Burkholderiaceae-related endobacterium impacts on sexual reproduction of its fungal host. Microbes Environ 35(2):ME19167
Taylor TN, Remy W, Hass H, Kerp H (1995) Fossil arbuscular mycorrhizae from the early Devonian. Mycologia 87(4):560–573
Tedersoo L, Sánchez-Ramírez S, Kõljalg U, Bahram M, Döring M, Schigel D, May T, Ryberg M, Abarenkov K (2018) High-level classification of the fungi and a tool for evolutionary ecological analyses. Fungal Divers 90(1):135–159
Telagathoti A, Probst M, Peintner U (2021) Habitat, snow-cover and soil pH, affect the distribution and diversity of mortierellaceae species and their associations to bacteria. Front Microbiol 12:1817
Tisserant E, Malbreil M, Kuo A, Kohler A, Symeonidi A, Balestrini R, Charron P, Duensing N, Freidit Frey N, Gianinazzi-Pearson V, Gilbert LB, Handa Y, Herr JR, Hijri M, Koul R, Kawaguchi M, Krajinski F, Lammers PJ, Masclaux FG, Murat C, Morin E, Ndikumana S, Pagni M, Petitpierre D, Requena N, Rosikiewicz P, Riley R, Saito K, San Clemente H, Shapiro H, van Tuinen D, Becard G, Bonfante P, Paszkowski U, Shachar-Hill YY, Tuskan GA, Young JP, Sanders IR, Henrissat B, Rensing SA, Grigoriev IV, Corradi N, Roux C, Martin F (2013) Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis. Proc Natl Acad Sci U S A 110(50):20117–20122. https://doi.org/10.1073/pnas.1313452110
Toomer KH, Chen X, Naito M, Mondo SJ, den Bakker HC, VanKuren NW, Lekberg Y, Morton JB, Pawlowska TE (2015) Molecular evolution patterns reveal life history features of mycoplasma-related endobacteria associated with arbuscular mycorrhizal fungi. Mol Ecol 24(13):3485–3500
Torres-Cortes G, Ghignone S, Bonfante P, Schussler A (2015) Mosaic genome of endobacteria in arbuscular mycorrhizal fungi: Transkingdom gene transfer in an ancient mycoplasma-fungus association. Proc Natl Acad Sci U S A 112(25):7785–7790. https://doi.org/10.1073/pnas.1501540112
Torres-Cruz TJ, Billingsley Tobias TL, Almatruk M, Hesse CN, Kuske CR, Desirò A, Benucci GMN, Bonito G, Stajich JE, Dunlap C (2017) Bifiguratus adelaidae, gen. Et sp. nov., a new member of Mucoromycotina in endophytic and soil-dwelling habitats. Mycologia 109(3):363–378
Turina M, Ghignone S, Astolfi N, Silvestri A, Bonfante P, Lanfranco L (2018) The virome of the arbuscular mycorrhizal fungus Gigaspora margarita reveals the first report of DNA fragments corresponding to replicating non-retroviral RNA viruses in fungi. Environ Microbiol 20(6):2012–2025
Uehling J, Gryganskyi A, Hameed K, Tschaplinski T, Misztal P, Wu S, Desirò A, Vande Pol N, Du Z, Zienkiewicz A (2017) Comparative genomics of Mortierella elongata and its bacterial endosymbiont Mycoavidus cysteinexigens. Environ Microbiol 19(8):2964–2983
Uzum Z, Silipo A, Lackner G, De Felice A, Molinaro A, Hertweck C (2015) Structure, genetics and function of an exopolysaccharide produced by a bacterium living within fungal hyphae. Chembiochem 16(3):387–392
Vandepol N, Liber J, Desirò A, Na H, Kennedy M, Barry K, Grigoriev IV, Miller AN, O’Donnell K, Stajich JE (2020) Resolving the Mortierellaceae phylogeny through synthesis of multi-gene phylogenetics and phylogenomics. Fungal Divers 104(1):267–289
VanKuren NW, den Bakker HC, Morton JB, Pawlowska TE (2013) Ribosomal RNA gene diversity, effective population size, and evolutionary longevity in asexual Glomeromycota. Evolution: international journal of organic. Evolution 67(1):207–224
Vannini C, Carpentieri A, Salvioli A, Novero M, Marsoni M, Testa L, Pinto MC, Amoresano A, Ortolani F, Bracale M (2016) An interdomain network: the endobacterium of a mycorrhizal fungus promotes antioxidative responses in both fungal and plant hosts. New Phytol 211(1):265–275
Venice F, Ghignone S, Salvioli di Fossalunga A, Amselem J, Novero M, Xianan X, Sędzielewska Toro K, Morin E, Lipzen A, Grigoriev IV (2020a) At the nexus of three kingdoms: the genome of the mycorrhizal fungus Gigaspora margarita provides insights into plant, endobacterial and fungal interactions. Environ Microbiol 22(1):122–141
Venice F, Desirò A, Silva G, Salvioli A, Bonfante P (2020b) The mosaic architecture of NRPS-PKS in the arbuscular mycorrhizal fungus gigaspora margarita shows a domain with bacterial signature. Front Microbiol 11:581313
Venice F, Chialva M, Domingo G, Novero M, Carpentieri A, Salvioli di Fossalunga A, Ghignone S, Amoresano A, Vannini C, Lanfranco L (2021) Symbiotic responses of Lotus japonicus to two isogenic lines of a mycorrhizal fungus differing in the presence/absence of an endobacterium. Plant J 108(6):1547–1564
Walker C (1985) Endogone lactiflua forming ectomycorrhizas with Pinus contorta. Trans Br Mycol Soc 84(2):353–355
Walker C, Gollotte A, Redecker D (2018) A new genus, Planticonsortium (Mucoromycotina), and new combination (P. tenue), for the fine root endophyte, Glomus tenue (basionym Rhizophagus tenuis). Mycorrhiza 28(3):213–219
Walsh TJ, Gamaletsou MN, McGinnis MR, Hayden RT, Kontoyiannis DP (2012) Early clinical and laboratory diagnosis of invasive pulmonary, extrapulmonary, and disseminated mucormycosis (zygomycosis). Clin Infect Dis 54(suppl_1):S55–S60
Warcup J (1990) Taxonomy, culture and mycorrhizal associations of some zygosporic Endogonaceae. Mycol Res 94(2):173–178
Wiersinga WJ, Van der Poll T, White NJ, Day NP, Peacock SJ (2006) Melioidosis: insights into the pathogenicity of Burkholderia pseudomallei. Nat Rev Microbiol 4(4):272–282
Wurlitzer JM, Stanišić A, Wasmuth I, Jungmann S, Fischer D, Kries H, Gressler M (2021) Bacterial-like nonribosomal peptide synthetases produce cyclopeptides in the zygomycetous fungus Mortierella alpina. Appl Environ Microbiol 87(3):e02051–e02020
Yamamoto K, Endo N, Degawa Y, Fukuda M, Yamada A (2017) First detection of Endogone ectomycorrhizas in natural oak forests. Mycorrhiza 27(3):295–301
Yang S, Anikst V, Adamson PC (2022) Endofungal Mycetohabitans rhizoxinica Bacteremia associated with Rhizopus microsporus respiratory tract infection. Emerg Infect Dis 28(10):2091
Acknowledgments
The authors would like to acknowledge the following funding sources for supporting this work: Support was provided by NSF 2202410, NSF 2030338 to JKU, DOESFA LANLF59T, NSF 1737898 to GB, and Conacyt FOINS-2015-01-006 to LPPM.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2023 The Author(s), under exclusive license to Springer Nature Switzerland AG
About this chapter
Cite this chapter
Uehling, J.K., Salvioli, A., Amses, K.R., Partida-Martínez, L.P., Bonito, G., Bonfante, P. (2023). Bacterial Endosymbionts of Mucoromycota Fungi: Diversity and Function of their Interactions. In: Pöggeler, S., James, T. (eds) Evolution of Fungi and Fungal-Like Organisms. The Mycota, vol 14. Springer, Cham. https://doi.org/10.1007/978-3-031-29199-9_8
Download citation
DOI: https://doi.org/10.1007/978-3-031-29199-9_8
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-031-29198-2
Online ISBN: 978-3-031-29199-9
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)