Deep space and hidden depths: understanding the evolution and ecology of fungal entomopathogens

Roy, Helen E.; Brodie, Eoin L.; Chandler, Dave; Goettel, Mark S.; Pell, J. K.; Wajnberg, Éric; Vega, Fernando E.

doi:10.1007/s10526-009-9244-7

Cited by 30 publications

(8 citation statements)

References 38 publications

(47 reference statements)

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“…The fungal pathogen Pandora neoaphidus (Zygomycota: Entomophthorales) is another specialized, widespread, and important natural enemy of the pea aphid acting as an effective natural biological control of pea aphid populations (57,58). The P. neoaphidis (genotype ARSEF 2588) used in this study originated from the USDAARS Collection of Entomopathogenic Fungal Cultures.…”

Section: Methodsmentioning

confidence: 99%

Aphid Heritable Symbiont Exploits Defensive Mutualism

Doremus

Oliver

2017

Appl Environ Microbiol

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Insects and other animals commonly form symbioses with heritable bacteria, which can exert large influences on host biology and ecology. The pea aphid, Acyrthosiphon pisum, is a model for studying effects of infection with heritable facultative symbionts (HFS), and each of its seven common HFS species has been reported to provide resistance to biotic or abiotic stresses. However, one common HFS, called X-type, rarely occurs as a single infection in field populations and instead typically superinfects individual aphids with Hamiltonella defensa, another HFS that protects aphids against attack by parasitic wasps. Using experimental aphid lines comprised of all possible infection combinations in a uniform aphid genotype, we investigated whether the most common strain of X-type provides any of the established benefits associated with aphid HFS as a single infection or superinfection with H. defensa. We found that X-type does not confer protection to any tested threats, including parasitoid wasps, fungal pathogens, or thermal stress. Instead, component fitness assays identified large costs associated with X-type infection, costs which were ameliorated in superinfected aphids. Together these findings suggest that X-type exploits the aphid/H. defensa mutualism and is maintained primarily as a superinfection by "hitchhiking" via the mutualistic benefits provided by another HFS. Exploitative symbionts potentially restrict the functions and distributions of mutualistic symbioses with effects that extend to other community members.IMPORTANCE Maternally transmitted bacterial symbionts are widespread and can have major impacts on the biology of arthropods, including insects of medical and agricultural importance. Given that host fitness and symbiont fitness are tightly linked, inherited symbionts can spread within host populations by providing beneficial services. Many insects, however, are frequently infected with multiple heritable symbiont species, providing potential alternative routes of symbiont maintenance. Here we show that a common pea aphid symbiont called X-type likely employs an exploitative strategy of hitchhiking off the benefits of a protective symbiont, Hamiltonella. Infection with X-type provides none of the benefits conferred by other aphid symbionts and instead results in large fitness costs, costs lessened by superinfection with Hamiltonella. These findings are corroborated by natural infections in field populations, where X-type is mostly found superinfecting aphids with Hamiltonella. Exploitative symbionts may be common in hosts with communities of heritable symbionts and serve to hasten the breakdown of mutualisms.KEYWORDS Hamiltonella defensa, PAXS, entomopathogenic fungi, heat stress, heritable symbionts, parasitoids, pea aphid resistance H eritable bacterial symbionts are ubiquitous in arthropod species, especially insects occupying terrestrial ecosystems (1). These heritable symbionts are usually maternally transmitted and cannot survive outside host tissues and consequently have limited s...

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Section: Methodsmentioning

confidence: 99%

Aphid Heritable Symbiont Exploits Defensive Mutualism

Doremus

Oliver

2017

Appl Environ Microbiol

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“…A likely scenario appears to be that the fungus uses the plant as vector, that is, to enhance its transmission rate among different insect hosts. Knowledge on the ecology of these entomopathogens is limited (Rodriguez et al, 2009; Vega et al, 2009; Roy et al, 2010) and it therefore remains to be proven whether the negative effects on insect hosts can positively feed back to plant fitness. However, “biocontrol” entomopathogens are commonly isolated from symptomless plant tissues (Ownley et al, 2010) and beyond doubt can kill their insect hosts, which makes it likely that they exhibit a positive effects at least at the level of plant populations.…”

Section: Major Endophyte Groups and Their Positive Effects On Host Plmentioning

confidence: 99%

The Microbe-Free Plant: Fact or Artifact?

Partida‐Martínez¹,

Heil²

2011

Front. Plant Sci.

300

180

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Plant–microbe interactions are ubiquitous. Plants are threatened by pathogens, but they are even more commonly engaged in neutral or mutualistic interactions with microbes: belowground microbial plant associates are mycorrhizal fungi, Rhizobia, and plant-growth promoting rhizosphere bacteria, aboveground plant parts are colonized by internally living bacteria and fungi (endophytes) and by microbes in the phyllosphere (epiphytes). We emphasize here that a completely microbe-free plant is an exotic exception rather than the biologically relevant rule. The complex interplay of such microbial communities with the host–plant affects multiple vital parameters such as plant nutrition, growth rate, resistance to biotic and abiotic stressors, and plant survival and distribution. The mechanisms involved reach from direct ones such as nutrient acquisition, the production of plant hormones, or direct antibiosis, to indirect ones that are mediated by effects on host resistance genes or via interactions at higher trophic levels. Plant-associated microbes are heterotrophic and cause costs to their host plant, whereas the benefits depend on the current environment. Thus, the outcome of the interaction for the plant host is highly context dependent. We argue that considering the microbe-free plant as the “normal” or control stage significantly impairs research into important phenomena such as (1) phenotypic and epigenetic plasticity, (2) the “normal” ecological outcome of a given interaction, and (3) the evolution of plants. For the future, we suggest cultivation-independent screening methods using direct PCR from plant tissue of more than one fungal and bacterial gene to collect data on the true microbial diversity in wild plants. The patterns found could be correlated to host species and environmental conditions, in order to formulate testable hypotheses on the biological roles of plant endophytes in nature. Experimental approaches should compare different host–endophyte combinations under various relevant environmental conditions and study at the genetic, epigenetic, transcriptional, and physiological level the parameters that cause the interaction to shift along the mutualism–parasitism continuum.

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“…However, the wealth of literature on the role of such fungal entomopathogens in controlling pest insects is countered by a lack of basic ecological understanding on aspects such as their distribution in natural habitats (Meyling et al, 2009;Roy et al, 2009Roy et al, , 2010Vega et al, 2009;Hesketh et al, 2010). However, the wealth of literature on the role of such fungal entomopathogens in controlling pest insects is countered by a lack of basic ecological understanding on aspects such as their distribution in natural habitats (Meyling et al, 2009;Roy et al, 2009Roy et al, , 2010Vega et al, 2009;Hesketh et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

A fungal pathogen in time and space: the population dynamics of Beauveria bassiana in a conifer forest

Ormond

Thomas

Pugh

et al. 2010

FEMS Microbiology Ecology

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The fungal entomopathogen Beauveria bassiana is ubiquitous in below-ground systems; however, there is a dearth of information on the above-ground diversity, temporal and spatial distribution of this fungus. Therefore, we assessed its occurrence in a conifer forest (Pseudotsuga monziesii and Pinus nigra var. maritima) using selective media to isolate B. bassiana from soil, branch and bark samples collected in October 2005, March and June 2006. Fungal density was the highest at all locations in October, declining in March and June, and absent from conifer branches in June. This above-ground decline most likely resulted from more extreme environmental conditions compared with those below ground. Molecular analyses (ISSR-PCR) indicated that B. bassiana is genetically diverse, comprising both distinct microhabitat-specific and seasonal isolates. The occurrence of dissimilar above- and below-ground isolates suggests that B. bassiana occupies various overlapping niches in these systems.

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Deep space and hidden depths: understanding the evolution and ecology of fungal entomopathogens

Cited by 30 publications

References 38 publications

Aphid Heritable Symbiont Exploits Defensive Mutualism

Aphid Heritable Symbiont Exploits Defensive Mutualism

The Microbe-Free Plant: Fact or Artifact?

A fungal pathogen in time and space: the population dynamics of Beauveria bassiana in a conifer forest

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