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Made for Each Other: Ascomycete Yeasts and Insects

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  • Author: Meredith Blackwell1
  • Editors: Joseph Heitman2, Neil A. R. Gow3
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Departments of Biological Sciences, Louisiana State University, Baton Rouge, LA 70803 and University of South Carolina, Columbia, SC 29208; 2: Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, NC 27710; 3: School of Medical Sciences, University of Aberdeen, Fosterhill, Aberdeen, AB25 2ZD, United Kingdom
  • Source: microbiolspec June 2017 vol. 5 no. 3 doi:10.1128/microbiolspec.FUNK-0081-2016
  • Received 02 July 2016 Accepted 14 December 2016 Published 09 June 2017
  • Meredith Blackwell, mblackwell@lsu.edu
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  • Abstract:

    Fungi and insects live together in the same habitats, and many species of both groups rely on each other for success. Insects, the most successful animals on Earth, cannot produce sterols, essential vitamins, and many enzymes; fungi, often yeast-like in growth form, make up for these deficits. Fungi, however, require constantly replenished substrates because they consume the previous ones, and insects, sometimes lured by volatile fungal compounds, carry fungi directly to a similar, but fresh, habitat. Yeasts associated with insects include Ascomycota (Saccharomycotina, Pezizomycotina) and a few Basidiomycota. Beetles, homopterans, and flies are important associates of fungi, and in turn the insects carry yeasts in pits, specialized external pouches, and modified gut pockets. Some yeasts undergo sexual reproduction within the insect gut, where the genetic diversity of the population is increased, while others, well suited to their stable environment, may never mate. The range of interactions extends from dispersal of yeasts on the surface of insects (e.g., cactus--yeast and ephemeral flower communities, ambrosia beetles, yeasts with holdfasts) to extremely specialized associations of organisms that can no longer exist independently, as in the case of yeast-like symbionts of planthoppers. In a few cases yeast-like fungus-insect associations threaten butterflies and other species with extinction. Technical advances improve discovery and identification of the fungi but also inform our understanding of the evolution of yeast-insect symbioses, although there is much more to learn.

  • Citation: Blackwell M. 2017. Made for Each Other: Ascomycete Yeasts and Insects. Microbiol Spectrum 5(3):FUNK-0081-2016. doi:10.1128/microbiolspec.FUNK-0081-2016.

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/content/journal/microbiolspec/10.1128/microbiolspec.FUNK-0081-2016
2017-06-09
2017-11-22

Abstract:

Fungi and insects live together in the same habitats, and many species of both groups rely on each other for success. Insects, the most successful animals on Earth, cannot produce sterols, essential vitamins, and many enzymes; fungi, often yeast-like in growth form, make up for these deficits. Fungi, however, require constantly replenished substrates because they consume the previous ones, and insects, sometimes lured by volatile fungal compounds, carry fungi directly to a similar, but fresh, habitat. Yeasts associated with insects include Ascomycota (Saccharomycotina, Pezizomycotina) and a few Basidiomycota. Beetles, homopterans, and flies are important associates of fungi, and in turn the insects carry yeasts in pits, specialized external pouches, and modified gut pockets. Some yeasts undergo sexual reproduction within the insect gut, where the genetic diversity of the population is increased, while others, well suited to their stable environment, may never mate. The range of interactions extends from dispersal of yeasts on the surface of insects (e.g., cactus--yeast and ephemeral flower communities, ambrosia beetles, yeasts with holdfasts) to extremely specialized associations of organisms that can no longer exist independently, as in the case of yeast-like symbionts of planthoppers. In a few cases yeast-like fungus-insect associations threaten butterflies and other species with extinction. Technical advances improve discovery and identification of the fungi but also inform our understanding of the evolution of yeast-insect symbioses, although there is much more to learn.

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Figures

Image of FIGURE 1
FIGURE 1

Many yeasts reproduce asexually by budding. from a culture. Scale bar = 5 μm. Photograph courtesy of N.H. Nguyen.

Source: microbiolspec June 2017 vol. 5 no. 3 doi:10.1128/microbiolspec.FUNK-0081-2016
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Image of FIGURE 2
FIGURE 2

The edge of a 9-cm plate showing discrete budding yeast colonies developed on agar after streaking. Photograph courtesy of S.-O. Suh.

Source: microbiolspec June 2017 vol. 5 no. 3 doi:10.1128/microbiolspec.FUNK-0081-2016
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Image of FIGURE 3
FIGURE 3

Hat-shaped ascospores of . Ascospore shape was once thought to be a good phylogenetic character in yeasts. DNA sequencing indicates it has arisen independently several times, not only in yeasts, but also in Pezizomycotina. Scale bar = 5 μm. Photograph courtesy of S.-O. Suh.

Source: microbiolspec June 2017 vol. 5 no. 3 doi:10.1128/microbiolspec.FUNK-0081-2016
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Image of FIGURE 4
FIGURE 4

(Passalidae). Partially dissected beetle shows the gut and its regions . (MG, midgut; PHG, posterior hindgut; AHG, anterior hindgut. Foregut (FG), MG, AHG, and PHG removed from the beetle. A surface film of attached bacteria is located in the differentiated AHG; is attached in the PHG (see Fig. 10 ) ( 78 ). Preparation and photograph courtesy of N.H. Nguyen.

Source: microbiolspec June 2017 vol. 5 no. 3 doi:10.1128/microbiolspec.FUNK-0081-2016
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Image of FIGURE 5
FIGURE 5

(Curculionidae: Scolytinae: Xyleborini). Large, complex bilobed mesonotal mycangium (stained blue) with opening on the pronotum; spores of the mycangial symbiont at the edge of the pronotum. Fungi in Ceratocystidaceae, including , have close associations with certain species of beetle and produce arthrospore-like cells rather than yeast-like budding typical of other ambrosial symbionts. Photograph courtesy of Chase G. Mayers.

Source: microbiolspec June 2017 vol. 5 no. 3 doi:10.1128/microbiolspec.FUNK-0081-2016
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Image of FIGURE 6
FIGURE 6

, a species of beetle (Erotylidae) with parental care; red speckled adult beside a late instar larva (grub) on white basidiocarp of a wood-decaying fungus in Bolivia. Photograph courtesy of J.V. McHugh.

Source: microbiolspec June 2017 vol. 5 no. 3 doi:10.1128/microbiolspec.FUNK-0081-2016
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Image of FIGURE 7
FIGURE 7

The name of the yeast genus recognizes Dr. Sung-Oui Suh for his studies of yeasts in the field and laboratory. Barro Colorado Island, Panama, July 2002. Photograph, M. Blackwell.

Source: microbiolspec June 2017 vol. 5 no. 3 doi:10.1128/microbiolspec.FUNK-0081-2016
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Image of FIGURE 8
FIGURE 8

Four yeast biologists (l. to r. Drs. Marc-André Lachance, Clete Kurtzman, Jack Fell, and Teun Boekhout) at a coffee break at a meeting to celebrate the centenary of the CBS-KNAW Fungal Biodiversity Centre (since February 10, 2017, known as the Westerdijk Fungal Biology Centre), Utrecht, The Netherlands, in Amsterdam, April 2004. The genus recognizes the research of Dr. Boekhout; all the others also have yeast genera named for them and are cited in this chapter. Photograph M. Blackwell.

Source: microbiolspec June 2017 vol. 5 no. 3 doi:10.1128/microbiolspec.FUNK-0081-2016
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Image of FIGURE 9
FIGURE 9

(NRRL Y-17632), an ambrosia fungus disseminated by insect vectors, was isolated from a beetle larva in wood. This species has been reported to be associated with lymexylid ship timber beetles. Asci with hat-shaped ascospores developed on agar, although budding cells and abundant hyphae are also produced under the cultural conditions. Hat-shaped ascospores are a convergent character (see Fig. 3 ). Scale bar = 10 μm. See reference 133 . Photograph courtesy of Cletus Kurtzman.

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Image of FIGURE 10
FIGURE 10

Water mount made without a cover slip of the interior hindgut of (Passalidae) showing several thalli attached along a furrow in the hindgut. Scale bar = 100 μm. See reference 77 .

Source: microbiolspec June 2017 vol. 5 no. 3 doi:10.1128/microbiolspec.FUNK-0081-2016
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Image of FIGURE 11
FIGURE 11

Brown planthopper, , feeding on a rice stem. The insect and YLS harbored in its fat body are obligately associated for essential nutritional resources. Photograph courtesy of Sylvia Villareal, International Rice Research Institute.

Source: microbiolspec June 2017 vol. 5 no. 3 doi:10.1128/microbiolspec.FUNK-0081-2016
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Image of FIGURE 12
FIGURE 12

Yeasts are usually studied from isolations made in petri dishes, and their life histories in nature are largely unknown. The yeast described as (CBS 8560) and the nematode have a unique phoretic relationship with the poplar borer beetle (Coleoptera, Cerambycidae, ) that would be unobserved in pure culture. The yeast uses its bifurcate basal cell as a holdfast to attach to the nematode, and they both fly away on a beetle to get to a fresh environment. Scanning electron micrograph, bar = 0.4 mm. See reference 120 . Courtesy of J. Kerrigan.

Source: microbiolspec June 2017 vol. 5 no. 3 doi:10.1128/microbiolspec.FUNK-0081-2016
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Image of FIGURE 13
FIGURE 13

Ascospores of sp. photographed 24 h after being placed on agar. No cover slip was used, so it looks a little foggy. The ascospore produced several conidia at the ascospore tip, and these budded several times more to produce yeast cells before hyphae elongate. The yeasts are likely dispersed over the new substrate by the mite, improving the chance of finding a suitable fungal host in this complex life history. Scale bar = 50 μm. M. Blackwell.

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Tables

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TABLE 1

Some common insect-yeast and YLS associations

Source: microbiolspec June 2017 vol. 5 no. 3 doi:10.1128/microbiolspec.FUNK-0081-2016

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