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Bacterial Endosymbionts: Master Modulators of Fungal Phenotypes

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  • Authors: Sarah J. Araldi-Brondolo1, Joseph Spraker2, Justin P. Shaffer3, Emma H. Woytenko4, David A. Baltrus6, Rachel E. Gallery7, A. Elizabeth Arnold8
  • Editors: Joseph Heitman10, Timothy Y. James11
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: School of Plant Sciences; 2: School of Plant Sciences; 3: School of Plant Sciences; 4: School of Plant Sciences; 5: Graduate Interdisciplinary Program in Genetics; 6: School of Plant Sciences; 7: School of Natural Resources and the Environment; 8: School of Plant Sciences; 9: Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ 85721; 10: Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, NC 27710; 11: Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI 48109-1048
  • Source: microbiolspec September 2017 vol. 5 no. 5 doi:10.1128/microbiolspec.FUNK-0056-2016
  • Received 16 June 2017 Accepted 22 July 2017 Published 22 September 2017
  • A. Elizabeth Arnold, arnold@ag.arizona.edu
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  • Abstract:

    The ecological modes of fungi are shaped not only by their intrinsic features and the environment in which they occur, but also by their interactions with diverse microbes. Here we explore the ecological and genomic features of diverse bacterial endosymbionts—endohyphal bacteria—that together are emerging as major determinants of fungal phenotypes and plant-fungi interactions. We first provide a historical perspective on the study of endohyphal bacteria. We then propose a functional classification of three main groups, providing an overview of their genomic, phylogenetic, and ecological traits. Last, we explore frontiers in the study of endohyphal bacteria, with special attention to those facultative and horizontally transmitted bacteria that associate with some of the most diverse lineages of fungi. Overall, our aim is to synthesize the rich literature from nearly 50 years of studies on endohyphal bacteria as a means to highlight potential applications and new research directions.

  • Citation: Araldi-Brondolo S, Spraker J, Shaffer J, Woytenko E, Baltrus D, Gallery R, Arnold A. 2017. Bacterial Endosymbionts: Master Modulators of Fungal Phenotypes. Microbiol Spectrum 5(5):FUNK-0056-2016. doi:10.1128/microbiolspec.FUNK-0056-2016.

Key Concept Ranking

Type IV Secretion Systems
0.425318
Type III Secretion System
0.4079483
Type VI Secretion System
0.4079483
Type III Secretion System
0.4079483
Type VI Secretion System
0.4079483
Type II Secretion System
0.4017518
0.425318

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/content/journal/microbiolspec/10.1128/microbiolspec.FUNK-0056-2016
2017-09-22
2017-10-17

Abstract:

The ecological modes of fungi are shaped not only by their intrinsic features and the environment in which they occur, but also by their interactions with diverse microbes. Here we explore the ecological and genomic features of diverse bacterial endosymbionts—endohyphal bacteria—that together are emerging as major determinants of fungal phenotypes and plant-fungi interactions. We first provide a historical perspective on the study of endohyphal bacteria. We then propose a functional classification of three main groups, providing an overview of their genomic, phylogenetic, and ecological traits. Last, we explore frontiers in the study of endohyphal bacteria, with special attention to those facultative and horizontally transmitted bacteria that associate with some of the most diverse lineages of fungi. Overall, our aim is to synthesize the rich literature from nearly 50 years of studies on endohyphal bacteria as a means to highlight potential applications and new research directions.

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Image of FIGURE 1
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 .

Source: microbiolspec September 2017 vol. 5 no. 5 doi:10.1128/microbiolspec.FUNK-0056-2016
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Image of FIGURE 2
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 38 ).

Source: microbiolspec September 2017 vol. 5 no. 5 doi:10.1128/microbiolspec.FUNK-0056-2016
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Image of FIGURE 3
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 48 ). 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.

Source: microbiolspec September 2017 vol. 5 no. 5 doi:10.1128/microbiolspec.FUNK-0056-2016
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Image of FIGURE 4
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 ( 38 ). 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 38 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 ( 79 ).

Source: microbiolspec September 2017 vol. 5 no. 5 doi:10.1128/microbiolspec.FUNK-0056-2016
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Image of FIGURE 5
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 ( 79 ).

Source: microbiolspec September 2017 vol. 5 no. 5 doi:10.1128/microbiolspec.FUNK-0056-2016
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Image of FIGURE 6
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.

Source: microbiolspec September 2017 vol. 5 no. 5 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.

Source: microbiolspec September 2017 vol. 5 no. 5 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 ( 43 ). 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 43 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 ( 79 ).

Source: microbiolspec September 2017 vol. 5 no. 5 doi:10.1128/microbiolspec.FUNK-0056-2016
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Tables

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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)

Source: microbiolspec September 2017 vol. 5 no. 5 doi:10.1128/microbiolspec.FUNK-0056-2016

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