Chapter 49 : Bacterial Endosymbionts: Master Modulators of Fungal Phenotypes

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From the saprotrophs that decay plant material to the pathogens and mutualists that shape plant population dynamics at local and regional scales, fungi are major drivers of ecosystem health, plant productivity, and sustainability in all major biomes ( ). The ecological roles of such fungi are driven by their own genomic and epigenetic architecture, as well as that of their hosts, often with strong influences from the environmental context in which such interactions occur ( ).

Citation: Araldi-Brondolo S, Spraker J, Shaffer J, Woytenko E, Baltrus D, Gallery R, Arnold A. 2017. Bacterial Endosymbionts: Master Modulators of Fungal Phenotypes, p 981-1004. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0056-2016
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Figure 1

Fungal phenotypes result from direct and indirect interactions of fungal genomes, host genomes, substrate characteristics, and the environment, as well as the genomes of EHB. These often dynamic interactions occur in the context of biotic communities that are shaped by an evolutionary and biogeographic context .

Citation: Araldi-Brondolo S, Spraker J, Shaffer J, Woytenko E, Baltrus D, Gallery R, Arnold A. 2017. Bacterial Endosymbionts: Master Modulators of Fungal Phenotypes, p 981-1004. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0056-2016
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Figure 2

Fluorescent hybridization microscopy showing endophytic sp. 9143 harboring the class 3 endohyphal bacterium sp. 9143. The image shows the TAMRA fluorophore with the DAPI counterstain (blue), highlighting fungal nuclear and mitochondrial DNA in addition to bacteria (yellow/green). (Reprinted from reference ).

Citation: Araldi-Brondolo S, Spraker J, Shaffer J, Woytenko E, Baltrus D, Gallery R, Arnold A. 2017. Bacterial Endosymbionts: Master Modulators of Fungal Phenotypes, p 981-1004. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0056-2016
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Figure 3

Fluorescence microscopy (400×) reveals successful reintroduction of the class 3 EHB sp. 9143 with the tdTomato construct into hyphae of sp. 9143. The same image under phase contrast. (Images reprinted with modification from reference ). Healthy and apparently axenic colony of sp. 9143 in which EHB are present but not visible without microscopy. Conidium of sp. 9143. Although EHB are widespread in the culture that produced such conidia, no conidial transmission (i.e., no vertical transmission) has been detected.

Citation: Araldi-Brondolo S, Spraker J, Shaffer J, Woytenko E, Baltrus D, Gallery R, Arnold A. 2017. Bacterial Endosymbionts: Master Modulators of Fungal Phenotypes, p 981-1004. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0056-2016
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Figure 4

Phylogenetic relationships of selected class 2 EHB (black squares) associated with Mucoromycota, class 3 EHB (bold text) in the and that associate with fungal endophytes in the Ascomycota, known bacteria (regular font), and bacterial endophytes (black circles). For fungal endophytes hosting class 3 EHB, taxon labels indicate the fungal genus, the plant species from which these fungi were obtained (, , , ), the location in which the host tree was growing (NC, North Carolina; UA, University of Arizona Campus Arboretum, Tucson, Arizona; CHU, M, and MTL, montane regions of Arizona), relevant GenBank accessions, and bacterial genotype groups (operational taxonomic units) based on 97% similarity of bacterial 16S rRNA ( ). Colored labels indicate genome size and GC content for class 2 EHB (red) and class 3 EHB (blue), with the latter highlighting that members of the same 16S rRNA operational taxonomic unit can differ markedly in their genomic traits. Boxes containing R and X indicate class 3 EHB that have been reassociated with cured hosts under laboratory conditions (R) and transferred successfully and stably into novel fungal hosts (X). Labels for bacterial endophytes are similar to those of EHB in fungal endophytes but lack fungal hosts, because these bacteria occurred directly in plant tissues. Phylogenetic reconstruction from reference depicts the results of a Bayesian analysis of 16S rRNA gene sequences. Branch support values indicate parsimony bootstrap values (≥70%; before slash) and Bayesian posterior probabilities (≥95%; after slash). Branches in bold indicate ≥70% neighbor-joining bootstrap values. Endohyphal listed here have since been reclassified as ( ).

Citation: Araldi-Brondolo S, Spraker J, Shaffer J, Woytenko E, Baltrus D, Gallery R, Arnold A. 2017. Bacterial Endosymbionts: Master Modulators of Fungal Phenotypes, p 981-1004. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0056-2016
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Figure 5

Context-dependence in the outcomes of interactions between class 3 EHB and foliar endophytes (rows) and meaningful phenotypic variation among symbiotic partners (columns). Cells reflect the significance and directionality of repeated-measures analyses of variance assessing growth of fungal strains containing EHB and clones that were cured of EHB by antibiotic treatment over 14 days on water agar (low nutrient), malt extract agar (high nutrient), lignin medium (with indulin as the sole carbon source), and cellulose medium (carboxymethylcellulose as the sole carbon source). Thermotolerance was assessed on two media at 36°C. Cellulase activity was measured as zone-of-clearing scaled by colony diameter. Orange cells indicate that the growth or cellulase activity of clones with EHB significantly exceeded that of cured clones. Blue cells indicate that the growth or cellulase activity of cured clones significantly exceeded that of clones with EHB. Gray boxes indicate no significant difference (ns) as a function of EHB status. Fungi in red differ only in the identity of their EHB, in that their fungal genotypes at the barcode locus are identical. The endohyphal listed here is now ( ).

Citation: Araldi-Brondolo S, Spraker J, Shaffer J, Woytenko E, Baltrus D, Gallery R, Arnold A. 2017. Bacterial Endosymbionts: Master Modulators of Fungal Phenotypes, p 981-1004. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0056-2016
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Figure 6

Significantly more mass is lost from surface-sterilized, senescent leaves of a focal tree () following inoculation with containing a class 3 EHB ( sp. 9143, marked with +) versus treatment with clones of the same fungus cured of its EHB (–). Reassociation of the EHB and fungus following curing (R) led to mass loss that did not differ significantly from the original EHB-fungi association. Data reflect 14 days postinoculation in moist chambers. Scaled mass loss is positively correlated with the quantity of visible hyphae on tissue (0 = no visible hyphae; 4 = 100% of foliage covered with fungal growth). Hyphal coverage (white) after 14 days on surface-sterilized, presenescent foliage of in moist chambers. Controls (water only) had no visible hyphal growth. Hyphal coverage in with EHB exceeded that of without the EHB.

Citation: Araldi-Brondolo S, Spraker J, Shaffer J, Woytenko E, Baltrus D, Gallery R, Arnold A. 2017. Bacterial Endosymbionts: Master Modulators of Fungal Phenotypes, p 981-1004. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0056-2016
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Figure 7

Class 3 EHB can modulate the establishment of endophytic fungi in healthy foliage. Surface-sterilized foliage of the focal tree species, , was immersed in a suspension containing axenic hyphae, a suspension containing hyphae with the EHB, or water only. Tubes were left in place for 24 h and then removed. Inoculated branches were marked with colored wire according to treatment. After 2 weeks, tissue was surface-sterilized and evaluated for endophytes. The foliar endophyte was reisolated from surface-sterilized, inoculated plant tissue (+, endophyte with EHB; –, axenic endophyte; R, reassociated EHB and endophyte). These strains do not differ in growth on standard media under laboratory conditions. Successful inoculation by the axenic endophyte (EHB–, gray) and especially by the endophyte with EHB (EHB+, black); axis shows percentage of 2-mm tissue segments from which the fungus was reisolated. The endophyte was never observed in untreated foliage (control, orange). *Host species from which focal symbiotic pair was first isolated.

Citation: Araldi-Brondolo S, Spraker J, Shaffer J, Woytenko E, Baltrus D, Gallery R, Arnold A. 2017. Bacterial Endosymbionts: Master Modulators of Fungal Phenotypes, p 981-1004. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0056-2016
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Figure 8

Genomic traits of class 3 EHB associated with foliar endophytes in the Ascomycota (blue font) compared with nonendohyphal relatives (black) and a model class 2 EHB (red), showing the bacterial habitat, genome size, gene count, and results of Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway searches to identify bacterial pathways involved in signaling between bacteria and eukaryotes ( ). Boxes along the axis indicate KEGG pathway identifiers (top) for constituent genes for each bacterial secretion system. Colored boxes indicate that at least one gene within the genome is present and classified according to that specific KEGG identifier. Numbers inside the colored boxes denote that more than one gene within that genome is classified according to that KEGG identifier. Boxes for EHB bacteria described first in reference are shown in blue. Green boxes highlight a species that interacts with fungi but does not appear to occur endohyphally. Endohyphal listed here are now reclassified as ( ).

Citation: Araldi-Brondolo S, Spraker J, Shaffer J, Woytenko E, Baltrus D, Gallery R, Arnold A. 2017. Bacterial Endosymbionts: Master Modulators of Fungal Phenotypes, p 981-1004. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0056-2016
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1. Rodriguez RJ,, White JF Jr,, Arnold AE,, Redman RS . 2009. Fungal endophytes: diversity and functional roles. New Phytol 182 : 314 330.[CrossRef] [PubMed]
2. Rodriguez RJ,, Henson J,, Van Volkenburgh E,, Hoy M,, Wright L,, Beckwith F,, Kim Y-O,, Redman RS . 2008. Stress tolerance in plants via habitat-adapted symbiosis. ISME J 2 : 404 416.[CrossRef] [PubMed]
3. Saunders M,, Glenn AE,, Kohn LM . 2010. Exploring the evolutionary ecology of fungal endophytes in agricultural systems: using functional traits to reveal mechanisms in community processes. Evol Appl 3 : 525 537.[CrossRef] [PubMed]
4. Friesen ML,, Porter SS,, Stark SC,, von Wettberg EJ,, Sachs JL,, Martinez-Romero E . 2011. Microbially mediated plant functional traits. Annu Rev Ecol Evol Syst 42 : 23 46.[CrossRef]
5. Podolich O,, Ardanov P,, Zaets I,, Pirttilä AM,, Kozyrovska N . 2015. Reviving of the endophytic bacterial community as a putative mechanism of plant resistance. Plant Soil 388 : 367 377.[CrossRef]
6. Boer W,, Folman LB,, Summerbell RC,, Boddy L . 2005. Living in a fungal world: impact of fungi on soil bacterial niche development. FEMS Microbiol Rev 29 : 795 811.[CrossRef] [PubMed]
7. Worchel ER,, Giauque HE,, Kivlin SN . 2013. Fungal symbionts alter plant drought response. Microb Ecol 65 : 671 678.[CrossRef] [PubMed]
8. D’Alessandro M,, Erb M,, Ton J,, Brandenburg A,, Karlen D,, Zopfi J,, Turlings TCJ . 2014. Volatiles produced by soil-borne endophytic bacteria increase plant pathogen resistance and affect tritrophic interactions. Plant Cell Environ 37 : 813 826.[CrossRef] [PubMed]
9. Hardoim PR,, van Overbeek LS,, Berg G,, Pirttilä AM,, Compant S,, Campisano A,, Döring M,, Sessitsch A . 2015. The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol Mol Biol Rev 79 : 293 320.[CrossRef] [PubMed]
10. Roossinck MJ . 2015. Metagenomics of plant and fungal viruses reveals an abundance of persistent lifestyles. Front Microbiol 5 : 767.[CrossRef] [PubMed]
11. Hoffman MT,, Gunatilaka MK,, Wijeratne K,, Gunatilaka L,, Arnold AE . 2013. Endohyphal bacterium enhances production of indole-3-acetic acid by a foliar fungal endophyte. PLoS One 8 : e73132.[CrossRef] [PubMed]
12. Benoit I,, van den Esker MH,, Patyshakuliyeva A,, Mattern DJ,, Blei F,, Zhou M,, Dijksterhuis J,, Brakhage AA,, Kuipers OP,, de Vries RP,, Kovács AT . 2015. Bacillus subtilis attachment to Aspergillus niger hyphae results in mutually altered metabolism. Environ Microbiol 17 : 2099 2113.[CrossRef] [PubMed]
13. Salvioli A,, Ghignone S,, Novero M,, Navazio L,, Venice F,, Bagnaresi P,, Bonfante P . 2016. Symbiosis with an endobacterium increases the fitness of a mycorrhizal fungus, raising its bioenergetic potential. ISME J 10 : 130 144.[CrossRef] [PubMed]
14. Partida-Martinez LP,, Hertweck C . 2005. Pathogenic fungus harbours endosymbiotic bacteria for toxin production. Nature 437 : 884 888.[CrossRef] [PubMed]
15. Lumini E,, Ghignone S,, Bianciotto V,, Bonfante P . 2006. Endobacteria or bacterial endosymbionts? To be or not to be. New Phytol 170 : 205 208.[CrossRef] [PubMed]
16. 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 : 583 609.[CrossRef] [PubMed]
17. Arendt KR . 2015. Symbiosis establishment and ecological effects of endohyphal bacteria on foliar fungi. Master’s thesis. University of Arizona.
18. Obasa K,, White FF,, Fellers J,, Kennelly M,, Liu S,, Katz B,, Tomich J,, Moore D,, Shinogle H,, Kelley K . 2017. A dimorphic and virulence-enhancing endosymbiont bacterium discovered in Rhizoctonia solani . Phytobiomes 1 : 14 23.[CrossRef]
19. Shaffer JP,, U’Ren JM,, Gallery RE,, Baltrus DA,, Arnold AE . 2017. An endohyphal bacterium ( Chitinophaga, Bacteroidetes) alters carbon source use by Fusarium keratoplasticum (F. solani species complex, Nectriaceae). Front Microbiol 8 : 350.[CrossRef] [PubMed]
20. de Bary HA . 1879. Die Erscheinung der Symbiose. Verlag von Karl J. Trübner, Strasbourg, Germany.
21. Son M,, Yu J,, Kim K-H . 2015. Five questions about mycoviruses. PLoS Pathog 11 : e1005172.[CrossRef] [PubMed]
22. Nuss DL . 2005. Hypovirulence: mycoviruses at the fungal-plant interface. Nat Rev Microbiol 3 : 632 642.[CrossRef] [PubMed]
23. Roossinck MJ . 2011. The good viruses: viral mutualistic symbioses. Nat Rev Microbiol 9 : 99 108.[CrossRef] [PubMed]
24. Márquez LM,, Roossinck MJ . 2012. Do persistent RNA viruses fit the trade-off hypothesis of virulence evolution? Curr Opin Virol 2 : 556 560.[CrossRef] [PubMed]
25. Ghabrial SA,, Castón JR,, Jiang D,, Nibert ML,, Suzuki N . 2015. 50-plus years of fungal viruses. Virology 479–480 : 356 368.[CrossRef] [PubMed]
26. Hillman BI,, Suzuki N . 2004. Viruses of the chestnut blight fungus, Cryphonectria parasitica . Adv Virus Res 62 : 423 462.
27. Bryner SF,, Rigling D,, Brunner PC . 2012. Invasion history and demographic pattern of Cryphonectria hypovirus 1 across European populations of the chestnut blight fungus. Ecol Evol 2 : 3227 3241.[CrossRef] [PubMed]
28. Xie J,, Jiang D . 2014. New insights into mycoviruses and exploration for the biological control of crop fungal diseases. Annu Rev Phytopathol 52 : 45 68.[CrossRef] [PubMed]
29. Pearson MN,, Bailey AM, . 2013. Viruses of Botrytis , p 251 272. In Ghabrial S (ed), Mycoviruses. Academic Press, San Diego, CA.[CrossRef] [PubMed]
30. Chu Y-M,, Jeon J-J,, Yea S-J,, Kim Y-H,, Yun S-H,, Lee Y-W,, Kim K-H . 2002. Double-stranded RNA mycovirus from Fusarium graminearum . Appl Environ Microbiol 68 : 2529 2534.[CrossRef] [PubMed]
31. Yu X,, Li B,, Fu Y,, Jiang D,, Ghabrial SA,, Li G,, Peng Y,, Xie J,, Cheng J,, Huang J,, Yi X . 2010. A geminivirus-related DNA mycovirus that confers hypovirulence to a plant pathogenic fungus. Proc Natl Acad Sci USA 107 : 8387 8392.[CrossRef] [PubMed]
32. Ro HS,, Lee NJ,, Lee CW,, Lee HS . 2006. Isolation of a novel mycovirus OMIV in Pleurotus ostreatus and its detection using a triple antibody sandwich-ELISA. J Virol Methods 138 : 24 29.[CrossRef] [PubMed]
33. Márquez LM,, Redman RS,, Rodriguez RJ,, Roossinck MJ . 2007. A virus in a fungus in a plant: three-way symbiosis required for thermal tolerance. Science 315 : 513 515.[CrossRef] [PubMed]
34. Chiba S,, Suzuki N . 2015. Highly activated RNA silencing via strong induction of dicer by one virus can interfere with the replication of an unrelated virus. Proc Natl Acad Sci USA 112 : E4911 E4918.[CrossRef] [PubMed]
35. Buck K, . 1998. Molecular variability of viruses of fungi, p 53 72. In Bridge P,, Couteaudier Y,, Clarkson JM (ed), Molecular Variability of Fungal Pathogens. CABI Press, Wallingford, United Kingdom.
36. Hammond TM,, Andrewski MD,, Roossinck MJ,, Keller NP . 2008. Aspergillus mycoviruses are targets and suppressors of RNA silencing. Eukaryot Cell 7 : 350 357.[CrossRef] [PubMed]
37. Liu S,, Xie J,, Cheng J,, Li B,, Chen T,, Fu Y,, Li G,, Wang M,, Jin H,, Wan H,, Jiang D . 2016. Fungal DNA virus infects a mycophagous insect and utilizes it as a transmission vector. Proc Natl Acad Sci USA 113 : 12803 12808.[CrossRef] [PubMed]
38. Hoffman MT,, Arnold AE . 2010. Diverse bacteria inhabit living hyphae of phylogenetically diverse fungal endophytes. Appl Environ Microbiol 76 : 4063 4075.[CrossRef] [PubMed]
39. Bonfante P . 2015. From environmental microbiology to ecogenomics: spotting the emerging field of fungal-bacterial interactions. Environ Microbiol Rep 7 : 15 17.[CrossRef] [PubMed]
40. Pawlowska TE, . 2016. Evolution in heritable bacterial: fungal endosymbioses, p 151 160. In Druzhinina IS,, Kubicek CP (ed), The Mycota, vol 4. Environmental and Microbial Relationships. Springer International Publishing, Cham, Germany.
41. 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 USA 112 : 7791 7796.[CrossRef] [PubMed]
42. Torres-Cortés G,, Ghignone S,, Bonfante P,, Schüßler A . 2015. Mosaic genome of endobacteria in arbuscular mycorrhizal fungi: transkingdom gene transfer in an ancient mycoplasma-fungus association. Proc Natl Acad Sci USA 112 : 7785 7790. (Erratum, 12:E5376.)[CrossRef]
43. Baltrus DA,, Dougherty K,, Arendt KR,, Huntemann M,, Clum A,, Pillay M,, Palaniappan K,, Varghese N,, Mikhailova N,, Stamatis D,, Reddy TBK,, Ngan CY,, Daum C,, Shapiro N,, Markowitz V,, Ivanova N,, Kyrpides N,, Woyke T,, Arnold AE . 2017. Absence of genome reduction in diverse, facultative endohyphal bacteria. Microb Genomics 3 : e000101.[CrossRef]
44. Uehling J,, Gryganskyi A,, Hameed K,, Tschaplinski T,, Misztal PK,, Wu S,, Desirò A,, Vande Pol N,, Du Z,, Zienkiewicz A,, Zienkiewicz K,, Morin E,, Tisserant E,, Splivallo R,, Hainaut M,, Henrissat B,, Ohm R,, Kuo A,, Yan J,, Lipzen A,, Nolan M,, LaButti K,, Barry K,, Goldstein AH,, Labbé J,, Schadt C,, Tuskan G,, Grigoriev I,, Martin F,, Vilgalys R,, Bonito G . 2017. Comparative genomics of Mortierella elongata and its bacterial endosymbiont Mycoavidus cysteinexigens . Environ Microbiol. [Epub ahead of print.][CrossRef]
45. Spatafora JW,, Chang Y,, Benny GL,, Lazarus K,, Smith ME,, Berbee ML,, Bonito G,, Corradi N,, Grigoriev I,, Gryganskyi A,, James TY,, O’Donnell K,, Roberson RW,, Taylor TN,, Uehling J,, Vilgalys R,, White MM,, Stajich JE . 2016. A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data. Mycologia 108 : 1028 1046.[CrossRef] [PubMed]
46. Bianciotto V,, Bandi C,, Minerdi D,, Sironi M,, Tichy HV,, Bonfante P . 1996. An obligately endosymbiotic mycorrhizal fungus itself harbors obligately intracellular bacteria. Appl Environ Microbiol 62 : 3005 3010.[PubMed]
47. Lackner G,, Möbius N,, Scherlach K,, Partida-Martinez LP,, Winkler R,, Schmitt I,, Hertweck C . 2009. Global distribution and evolution of a toxinogenic Burkholderia-Rhizopus symbiosis. Appl Environ Microbiol 75 : 2982 2986.[CrossRef] [PubMed]
48. Arendt KR,, Hockett KL,, Araldi-Brondolo SJ,, Baltrus DA,, Arnold AE . 2016. Isolation of endohyphal bacteria from foliar Ascomycota and in vitro establishment of their symbiotic associations. Appl Environ Microbiol 82 : 2943 2949.[CrossRef] [PubMed]
49. Shaffer JP,, Sarmiento C,, Zalamea P-C,, Gallery RE,, Davis AS,, Baltrus DA,, Arnold AE . 2016. Diversity, specificity, and phylogenetic relationships of endohyphal bacteria in fungi that inhabit tropical seeds and leaves. Front Ecol Evol 4 : 116.[CrossRef]
50. Ibrahim AS,, Gebremariam T,, Liu M,, Chamilos G,, Kontoyiannis D,, Mink R,, Kwon-Chung KJ,, Fu Y,, Skory CD,, Edwards JE Jr,, Spellberg B . 2008. Bacterial endosymbiosis is widely present among zygomycetes but does not contribute to the pathogenesis of mucormycosis. J Infect Dis 198 : 1083 1090.[CrossRef] [PubMed]
51. Partida-Martinez LP,, Bandemer S,, Rüchel R,, Dannaoui E,, Hertweck C . 2008. Lack of evidence of endosymbiotic toxin-producing bacteria in clinical Rhizopus isolates. Mycoses 51 : 266 269.[CrossRef] [PubMed]
52. Lackner G,, Hertweck C . 2011. Impact of endofungal bacteria on infection biology, food safety, and drug development. PLoS Pathog 7 : e1002096.[CrossRef] [PubMed]
53. MacDonald RM,, Chandler MR . 1981. Bacterium-like organelles in the vesicular-arbuscular mycorrhizal fungus Glomus caledonius . New Phytol 89 : 241 246.[CrossRef]
54. Protzenko MA . 1975. Micro-organism in the hyphae of mycorrhiza-forming fungus. Microbiologiya XLIV : 1121 1124.
55. Wilson JF,, Hanton WK . 1979. Bacteria-like structures in fungi, p 525 537. In Viruses and Plasmids in Fungi. Series on Mycology, Vol. 1. Marcel Dekker, New York, NY.
56. Kluge M,, Mollenhauer D,, Mollenhauer R,, Kape R . 1992. Geosiphon pyriforme, an endosymbiotic consortium of a fungus and a cyanobacterium ( Nostoc), fixes nitrogen. Bot Acta 105 : 343 344.[CrossRef]
57. 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. Bot Acta 107 : 36 45.[CrossRef]
58. Gehrig H,, Schüssler A,, Kluge M . 1996. Geosiphon pyriforme, a fungus forming endocytobiosis with Nostoc (cyanobacteria), is an ancestral member of the Glomales: evidence by SSU rRNA analysis. J Mol Evol 43 : 71 81.[CrossRef] [PubMed]
59. Kluge M . 2002. A fungus eats a cyanobacterium: the story of the Geosiphon pyriformis endocyanosis. Biol Environ Proc R Ir Acad 102 : 11 14.[CrossRef]
60. Ainsworth GC,, Sussman AS , (ed) . 1965. The Fungi: An Advanced Treatise, vol. 1, The Fungal Cell. Academic Press, San Diego, CA.
61. Langeron M,, Vanbreuseghem R . 1965. Outline of Mycology. Pitman Publishing, London, United Kingdom.
62. Carlile M,, Watkinson S . 1994. The Fungi, 3rd ed. Academic Press, London, United Kingdom.
63. Alexopoulos CJ,, Mims CW,, Blackwell M . 1996. Introductory Mycology, 4th ed. Wiley, Hoboken, NJ.
64. Bennett JW,, Feibelman T, . 2001. Fungal bacterial interactions, p 229 242. In Hock B (ed), The Mycota, vol. 9, Fungal Associations. Springer, Berlin, Germany.
65. Wolf FA,, Wolf FT . 1947. The Fungi, vol II. Wiley, Hoboken, NJ.
66. Mosse B . 1970. Honey-coloured, sessile endogone spores. II. Changes in fine structure during spore development. Arch Mikrobiol 74 : 129 145.[CrossRef]
67. Schrantz J . 1973. Presence of intracytoplasmic microorganisms, probably bacterial, in Discomycetes of genus Scuttelinia . C R Hebd Seances L Acad Sci 276 : 1541.
68. MacDonald RM,, Chandler MR,, Mosse B . 1982. The occurrence of bacterium-like organelles in vesicular-arbuscular mycorrhizal Fungi. New Phytol 90 : 659 663.[CrossRef]
69. Garbaye J . 1994. Helper bacteria: a new dimension to the mycorrhizal symbiosis. New Phytol 128 : 197 210.[CrossRef]
70. Wong PTW,, Griffin DM . 1976. Bacterial movement at high matric potentials? II. In fungal colonies. Soil Biol Biochem 8 : 219 223.[CrossRef]
71. Minerdi D,, Moretti M,, Gilardi G,, Barberio C,, Gullino ML,, Garibaldi A . 2008. Bacterial ectosymbionts and virulence silencing in a Fusarium oxysporum strain. Environ Microbiol 10 : 1725 1741.[CrossRef] [PubMed]
72. Honegger R . 1991. Functional aspects of the lichen symbiosis. Annu Rev Plant Physiol Plant Mol Biol 42 : 553 578.[CrossRef]
73. Young JM . 1970. Drippy gill: a bacterial disease of cultivated mushrooms caused by Pseudomonas agarici n.sp. N Z J Agric Res 13 : 977 990.[CrossRef]
74. Wong WC,, Fletcher JT,, Unsworth BA,, Preece TF . 1982. A note on ginger blotch, a new bacterial disease of the cultivated mushroom, Agaricus bisporus . J Appl Microbiol 52 : 43 48.
75. Campbell-Platt G . 1987. Fermented Foods of the World. A Dictionary and Guide. Butterworths Press, London, United Kingdom.
76. Scannerini S,, Bonfante-Fasolo P, . 1991. Bacteria and bacteria-like objects in endomycorrhizal fungi ( Glomaceae), p 273 287. In Margulis L,, Fester R (ed), Symbiosis as a Source of Evolutionary Innovation: Speciation and Morphogenesis. MIT Press, Cambridge, MA.
77. Scannerini S,, Bonfante P,, Fontana A, . 1975. An ultrastructural model for the host-symbiont interaction in the endotrophic mycorrhizae of Ornithogalum umbellatum L, p 314 324. In Sanders FE,, Mosse B,, Tinker PB (ed), Endomycorrhizas. Academic Press, New York, NY.
78. Bonfante-Fasolo P . 1987. Vesicular-arbuscular mycorrhizae: fungus-plant interactions at the cellular level. Symbiosis 3 : 249 268.
79. Sawana A,, Adeolu M,, Gupta RS . 2014. Molecular signatures and phylogenomic analysis of the genus Burkholderia: proposal for division of this genus into the emended genus Burkholderia containing pathogenic organisms and a new genus Paraburkholderia gen. nov. harboring environmental species. Front Genet 5 : 429.[CrossRef] [PubMed]
80. Bianciotto V,, Lumini E,, Lanfranco L,, Minerdi D,, Bonfante P,, Perotto S . 2000. Detection and identification of bacterial endosymbionts in arbuscular mycorrhizal fungi belonging to the family Gigasporaceae. Appl Environ Microbiol 66 : 4503 4509.[CrossRef] [PubMed]
81. Minerdi D,, Fani R,, Bonfante P, . 2002. Identification of putative Nifdk genes in the genome of a Burkholderia living in symbiosis with an arbuscular mycorrhizal fungus, p 206. In Pedrosa FO,, Hungria M,, Yates G,, Newton WE (ed), Nitrogen Fixation: From Molecules to Crop Productivity. Kluwer Academic Publishers, Dordrecht, The Netherlands.
82. Minerdi D,, Fani R,, Gallo R,, Boarino A,, Bonfante P . 2001. Nitrogen fixation genes in an endosymbiotic Burkholderia strain. Appl Environ Microbiol 67 : 725 732.[CrossRef] [PubMed]
83. 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 : 321 324.[CrossRef] [PubMed]
84. Bertaux J,, Schmid M,, Hutzler P,, Hartmann A,, Garbaye J,, Frey-Klett P . 2005. Occurrence and distribution of endobacteria in the plant-associated mycelium of the ectomycorrhizal fungus Laccaria bicolor S238N. Environ Microbiol 7 : 1786 1795.[CrossRef] [PubMed]
85. Sharma M,, Schmid M,, Rothballer M,, Hause G,, Zuccaro A,, Imani J,, Kämpfer P,, Domann E,, Schäfer P,, Hartmann A,, Kogel KH . 2008. Detection and identification of bacteria intimately associated with fungi of the order Sebacinales . Cell Microbiol 10 : 2235 2246.[CrossRef] [PubMed]
86. Bonfante P,, Anca I-A . 2009. Plants, mycorrhizal fungi, and bacteria: a network of interactions. Annu Rev Microbiol 63 : 363 383.[CrossRef] [PubMed]
87. Naumann M,, Schüssler A,, Bonfante P . 2010. The obligate endobacteria of arbuscular mycorrhizal fungi are ancient heritable components related to the Mollicutes. ISME J 4 : 862 871.[CrossRef] [PubMed]
88. 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 : 3485 3500.[CrossRef] [PubMed]
89. 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 : 257 270.[CrossRef] [PubMed]
90. Kuo C-H . 2015. Scrambled and not-so-tiny genomes of fungal endosymbionts. Proc Natl Acad Sci USA 112 : 7622 7623.[CrossRef] [PubMed]
91. 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 : 1177 1184.[CrossRef] [PubMed]
92. 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 : 822 836.[CrossRef] [PubMed]
93. 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 : 136 145.[CrossRef] [PubMed]
94. Barbieri E,, Riccioni G,, Pisano A,, Sisti D,, Zeppa S,, Agostini D,, Stocchi V . 2002. Competitive PCR for quantitation of a Cytophaga-Flexibacter-Bacteroides phylum bacterium associated with the Tuber borchii Vittad. mycelium. Appl Environ Microbiol 68 : 6421 6424.[CrossRef] [PubMed]
95. 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 : 248 257.[CrossRef] [PubMed]
96. 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 : 2052 2057.[CrossRef] [PubMed]
97. 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 : 121 124.[CrossRef] [PubMed]
98. Jargeat P,, Cosseau C,, Ola’h B,, Jauneau A,, Bonfante P,, Batut J,, Bécard 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 : 6876 6884.[CrossRef] [PubMed]
99. Partida-Martinez LP,, Flores de Looss C,, Ishida K,, Ishida M,, Roth M,, Buder K,, Hertweck C . 2007. Rhizonin, the first mycotoxin isolated from the zygomycota, is not a fungal metabolite but is produced by bacterial endosymbionts. Appl Environ Microbiol 73 : 793 797.[CrossRef] [PubMed]
100. Partida-Martinez LP,, Monajembashi S,, Greulich K-O,, Hertweck C . 2007. Endosymbiont-dependent host reproduction maintains bacterial-fungal mutualism. Curr Biol 17 : 773 777.[CrossRef] [PubMed]
101. Lackner G,, Partida-Martinez LP,, Hertweck C . 2009. Endofungal bacteria as producers of mycotoxins. Trends Microbiol 17 : 570 576.[CrossRef] [PubMed]
102. Barbieri E,, Potenza L,, Rossi I,, Sisti D,, Giomaro G,, Rossetti S,, Beimfohr C,, Stocchi V . 2000. Phylogenetic characterization and in situ detection of a Cytophaga-Flexibacter-Bacteroides phylogroup bacterium in Tuber borchii vittad. Ectomycorrhizal mycelium. Appl Environ Microbiol 66 : 5035 5042.[CrossRef] [PubMed]
103. Bianciotto V,, Genre A,, Jargeat P,, Lumini E,, Bécard G,, Bonfante P . 2004. Vertical transmission of endobacteria in the arbuscular mycorrhizal fungus Gigaspora margarita through generation of vegetative spores. Appl Environ Microbiol 70 : 3600 3608.[CrossRef] [PubMed]
104. 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 : 2083 2095.[PubMed]
105. Lumini E,, Bianciotto V,, Jargeat P,, Novero M,, Salvioli A,, Faccio A,, Bécard 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 : 1716 1729.[CrossRef] [PubMed]
106. Schmitt I,, Partida-Martinez LP,, Winkler R,, Voigt K,, Einax E,, Dölz F,, Telle S,, Wöstemeyer J,, Hertweck C . 2008. Evolution of host resistance in a toxin-producing bacterial-fungal alliance. ISME J 2 : 632 641.[CrossRef] [PubMed]
107. Lackner G,, Moebius N,, Partida-Martinez LP,, Boland S,, Hertweck C . 2011. Evolution of an endofungal lifestyle: deductions from the Burkholderia rhizoxinica genome. BMC Genomics 12 : 210.[CrossRef] [PubMed]
108. Moebius N,, Üzüm Z,, Dijksterhuis J,, Lackner G,, Hertweck C . 2014. Active invasion of bacteria into living fungal cells. eLife 3 : e03007.[CrossRef] [PubMed]
109. Partida-Martinez LP,, Groth I,, Schmitt I,, Richter W,, Roth M,, Hertweck C . 2007. Burkholderia rhizoxinica sp. nov. and Burkholderia endofungorum sp. nov., bacterial endosymbionts of the plant-pathogenic fungus Rhizopus microsporus . Int J Syst Evol Microbiol 57 : 2583 2590.[CrossRef] [PubMed]
110. 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 : e01272-14.[CrossRef] [PubMed]
111. Bonfante P,, Desirò A . 2017. Who lives in a fungus? The diversity, origins and functions of fungal endobacteria living in Mucoromycota. ISME J 11 : 1727 1735.[CrossRef] [PubMed]
112. 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 : 4243 4248.[CrossRef] [PubMed]
113. Qiang X,, Weiss M,, Kogel KH,, Schäfer P . 2012. Piriformospora indica: a mutualistic basidiomycete with an exceptionally large plant host range. Mol Plant Pathol 13 : 508 518.[CrossRef] [PubMed]
114. Glaeser SP,, Imani J,, Alabid I,, Guo H,, Kumar N,, Kämpfer P,, Hardt M,, Blom J,, Goesmann A,, Rothballer M,, Hartmann A,, Kogel K-H . 2016. Non-pathogenic Rhizobium radiobacter F4 deploys plant beneficial activity independent of its host Piriformospora indica . ISME J 10 : 871 884.[CrossRef] [PubMed]
115. Arnold AE,, Maynard Z,, Gilbert GS,, Coley PD,, Kursar TA . 2000. Are tropical fungal endophytes hyperdiverse? Ecol Lett 3 : 267 274.[CrossRef]
116. Arnold AE,, Miadlikowska J,, Higgins KL,, Sarvate SD,, Gugger P,, Way A,, Hofstetter V,, Kauff F,, Lutzoni F . 2009. A phylogenetic estimation of trophic transition networks for ascomycetous fungi: are lichens cradles of symbiotrophic fungal diversification? Syst Biol 58 : 283 297.[CrossRef] [PubMed]
117. Rohm B,, Scherlach K,, Möbius N,, Partida-Martinez LP,, Hertweck C . 2010. Toxin production by bacterial endosymbionts of a Rhizopus microsporus strain used for tempe/sufu processing. Int J Food Microbiol 136 : 368 371.[CrossRef] [PubMed]
118. Mela F,, Fritsche K,, de Boer W,, van Veen JA,, de Graaff LH,, van den Berg M,, Leveau JH . 2011. Dual transcriptional profiling of a bacterial/fungal confrontation: Collimonas fungivorans versus Aspergillus niger . ISME J 5 : 1494 1504.[CrossRef] [PubMed]
119. Deveau A,, Brulé C,, Palin B,, Champmartin D,, Rubini P,, Garbaye J,, Sarniguet A,, Frey-Klett P . 2010. Role of fungal trehalose and bacterial thiamine in the improved survival and growth of the ectomycorrhizal fungus Laccaria bicolor S238N and the helper bacterium Pseudomonas fluorescens BBc6R8. Environ Microbiol Rep 2 : 560 568.[CrossRef] [PubMed]
120. Deveau A,, Barret M,, Diedhiou AG,, Leveau J,, de Boer W,, Martin F,, Sarniguet A,, Frey-Klett P . 2015. Pairwise transcriptomic analysis of the interactions between the ectomycorrhizal fungus Laccaria bicolor S238N and three beneficial, neutral and antagonistic soil bacteria. Microb Ecol 69 : 146 159.[CrossRef] [PubMed]
121. Ochman H,, Lawrence JG,, Groisman EA . 2000. Lateral gene transfer and the nature of bacterial innovation. Nature 405 : 299 304.[CrossRef] [PubMed]
122. Fitzpatrick DA . 2012. Horizontal gene transfer in fungi. FEMS Microbiol Lett 329 : 1 8.[CrossRef] [PubMed]
123. Richards TA,, Leonard G,, Soanes DM,, Talbot NJ . 2011. Gene transfer into the fungi. Fungal Biol Rev 25 : 98 110.[CrossRef]
124. Lawrence DP,, Kroken S,, Pryor BM,, Arnold AE . 2011. Interkingdom gene transfer of a hybrid NPS/PKS from bacteria to filamentous Ascomycota. PLoS One 6 : e28231.[CrossRef] [PubMed]
125. de Groot MJ,, Bundock P,, Hooykaas PJ,, Beijersbergen AG . 1998. Agrobacterium tumefaciens-mediated transformation of filamentous fungi. Nat Biotechnol 16 : 839 842.[CrossRef] [PubMed]
126. Chuankun X,, Minghe M,, Leming Z,, Keqin Z . 2004. Soil volatile fungistasis and volatile fungistatic compounds. Soil Biol Biochem 36 : 1997 2004.[CrossRef]
127. Spraker JE,, Jewell K,, Roze LV,, Scherf J,, Ndagano D,, Beaudry R,, Linz JE,, Allen C,, Keller NP . 2014. A volatile relationship: profiling an inter-kingdom dialogue between two plant pathogens, Ralstonia Solanacearum and Aspergillus Flavus . J Chem Ecol 40 : 502 513.[CrossRef] [PubMed]
128. Stoppacher N,, Kluger B,, Zeilinger S,, Krska R,, Schuhmacher R . 2010. Identification and profiling of volatile metabolites of the biocontrol fungus Trichoderma atroviride by HS-SPME-GC-MS. J Microbiol Methods 81 : 187 193.[CrossRef] [PubMed]
129. Pennazza G,, Fanali C,, Santonico M,, Dugo L,, Cucchiarini L,, Dachà M,, D’Amico A,, Costa R,, Dugo P,, Mondello L . 2013. Electronic nose and GC-MS analysis of volatile compounds in Tuber magnatum Pico: evaluation of different storage conditions. Food Chem 136 : 668 674.[CrossRef] [PubMed]
130. Tognon G,, Campagnoli A,, Pinotti L,, Dell’Orto V,, Cheli F . 2005. Implementation of the electronic nose for the identification of mycotoxins in durum wheat ( Triticum durum). Vet Res Commun 29( Suppl 2) : 391 393.[CrossRef] [PubMed]
131. Pallottino F,, Costa C,, Antonucci F,, Strano MC,, Calandra M,, Solaini S,, Menesatti P . 2012. Electronic nose application for determination of Penicillium digitatum in Valencia oranges. J Sci Food Agric 92 : 2008 2012.[CrossRef] [PubMed]
132. Campagnoli A,, Cheli F,, Savoini G,, Crotti A,, Pastori AG,, Dell’Orto V . 2009. Application of an electronic nose to detection of aflatoxins in corn. Vet Res Commun 33( Suppl 1) : 273 275.[CrossRef] [PubMed]
133. Splivallo R,, Ottonello S,, Mello A,, Karlovsky P . 2011. Truffle volatiles: from chemical ecology to aroma biosynthesis. New Phytol 189 : 688 699.[CrossRef] [PubMed]
134. Watrous JD,, Dorrestein PC . 2011. Imaging mass spectrometry in microbiology. Nat Rev Microbiol 9 : 683 694.[CrossRef] [PubMed]
135. Spraker JE,, Sanchez LM,, Lowe TM,, Dorrestein PC,, Keller NP . 2016. Ralstonia solanacearum lipopeptide induces chlamydospore development in fungi and facilitates bacterial entry into fungal tissues. ISME J 10 : 2317 2330.[CrossRef] [PubMed]
136. Moree WJ,, Phelan VV,, Wu C-H,, Bandeira N,, Cornett DS,, Duggan BM,, Dorrestein PC . 2012. Interkingdom metabolic transformations captured by microbial imaging mass spectrometry. Proc Natl Acad Sci USA 109 : 13811 13816.[CrossRef] [PubMed]
137. Laskin J,, Heath BS,, Roach PJ,, Cazares L,, Semmes OJ . 2012. Tissue imaging using nanospray desorption electrospray ionization mass spectrometry. Anal Chem 84 : 141 148.[CrossRef] [PubMed]
138. Traxler MF,, Kolter R . 2012. A massively spectacular view of the chemical lives of microbes. Proc Natl Acad Sci USA 109 : 10128 10129.[CrossRef] [PubMed]
139. Watrous J,, Roach P,, Alexandrov T,, Heath BS,, Yang JY . 2012. Mass spectral molecular networking of living microbial colonies 109 : 1743 1752.
140. Levy A,, Chang BJ,, Abbott LK,, Kuo J,, Harnett G,, Inglis TJ . 2003. Invasion of spores of the arbuscular mycorrhizal fungus Gigaspora decipiens by Burkholderia spp. Appl Environ Microbiol 69 : 6250 6256.[CrossRef] [PubMed]
141. Grube M,, Berg G . 2009. Microbial consortia of bacteria and fungi with focus on the lichen symbiosis. Fungal Biol Rev 23 : 72 85.[CrossRef]
142. Stanley CE,, Stöckli M,, van Swaay D,, Sabotič J,, Kallio PT,, Künzler M,, deMello AJ,, Aebi M . 2014. Probing bacterial-fungal interactions at the single cell level. Integr Biol 6 : 935 945.[CrossRef] [PubMed]
143. Schmidt R,, Etalo DW,, de Jager V,, Gerards S,, Zweers H,, de Boer W,, Garbeva P . 2016. Microbial small talk: volatiles in fungal-bacterial interactions. Front Microbiol 6 : 1495.[CrossRef] [PubMed]
144. Effmert U,, Kalderás J,, Warnke R,, Piechulla B . 2012. Volatile mediated interactions between bacteria and fungi in the soil. J Chem Ecol 38 : 665 703.[CrossRef] [PubMed]
145. Mackie A,, Wheatley R . 1999. Effects and incidence of volatile organic compound interactions between soil bacterial and fungal isolates. Soil Biol Biochem 31 : 375 385.[CrossRef]
146. Wheatley RE . 2002. The consequences of volatile organic compound mediated bacterial and fungal interactions. Antonie van Leeuwenhoek 81 : 357 364.[CrossRef] [PubMed]
147. Pistole TG . 1981. Interaction of bacteria and fungi with lectins and lectin-like substances. Annu Rev Microbiol 35 : 85 112.[CrossRef] [PubMed]
148. Varrot A,, Basheer SM,, Imberty A . 2013. Fungal lectins: structure, function and potential applications. Curr Opin Struct Biol 23 : 678 685.[CrossRef] [PubMed]
149. Díaz EM,, Vicente-Manzanares M,, Sacristan M,, Vicente C,, Legaz M-E . 2011. Fungal lectin of Peltigera canina induces chemotropism of compatible Nostoc cells by constriction-relaxation pulses of cyanobiont cytoskeleton. Plant Signal Behav 6 : 1525 1536.[CrossRef] [PubMed]
150. Rudnick MB,, van Veen JA,, de Boer W . 2015. Baiting of rhizosphere bacteria with hyphae of common soil fungi reveals a diverse group of potentially mycophagous secondary consumers. Soil Biol Biochem 88 : 73 82.[CrossRef]
151. Salyers AA,, Reeves A,, D’Elia J . 1996. Solving the problem of how to eat something as big as yourself: diverse bacterial strategies for degrading polysaccharides. J Ind Microbiol Biotechnol 17 : 470 476.[CrossRef]
152. De Boer W,, Klein Gunnewiek PJA,, Lafeber P,, Janse JD,, Spit BE,, Woldendorp JW . 1997. Anti-fungal properties of chitinolytic dune soil bacteria. Soil Biol Biochem 30 : 193 203.[CrossRef]
153. Sajben E,, Manczinger L,, Nagy A,, Kredics L,, Vágvölgyi C . 2011. Characterization of pseudomonads isolated from decaying sporocarps of oyster mushroom. Microbiol Res 166 : 255 267.[CrossRef] [PubMed]
154. Soler-Rivas C,, Jolivet S,, Arpin N,, Olivier JM,, Wichers HJ . 1999. Biochemical and physiological aspects of brown blotch disease of Agaricus bisporus . FEMS Microbiol Rev 23 : 591 614.[CrossRef] [PubMed]
155. Cusano AM,, Burlinson P,, Deveau A,, Vion P,, Uroz S,, Preston GM,, Frey-Klett P . 2011. Pseudomonas fluorescens BBc6R8 type III secretion mutants no longer promote ectomycorrhizal symbiosis. Environ Microbiol Rep 3 : 203 210.[CrossRef] [PubMed]
156. Tzfira T,, Citovsky V . 2000. From host recognition to T-DNA integration: the function of bacterial and plant genes in the Agrobacterium-plant cell interaction. Mol Plant Pathol 1 : 201 212.[CrossRef] [PubMed]
157. Costa TRD,, Felisberto-Rodrigues C,, Meir A,, Prevost MS,, Redzej A,, Trokter M,, Waksman G . 2015. Secretion systems in Gram-negative bacteria: structural and mechanistic insights. Nat Rev Microbiol 13 : 343 359.[CrossRef] [PubMed]
158. Bingle LE,, Bailey CM,, Pallen MJ . 2008. Type VI secretion: a beginner’s guide. Curr Opin Microbiol 11 : 3 8.[CrossRef] [PubMed]


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Table 1

Functional classification of endohyphal bacteria into three operational classes based on host information, bacterial phylogeny, genomic traits, and associated traits relevant to bacteria/fungi interactions and ecology (references listed in text)

Citation: Araldi-Brondolo S, Spraker J, Shaffer J, Woytenko E, Baltrus D, Gallery R, Arnold A. 2017. Bacterial Endosymbionts: Master Modulators of Fungal Phenotypes, p 981-1004. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0056-2016

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