Microbial evolution and transitions along the parasite–mutualist continuum

Drew, Georgia C; Stevens, Emily; King, Kayla C.

doi:10.1038/s41579-021-00550-7

Cited by 207 publications

(165 citation statements)

References 255 publications

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“…Therefore, another unknown effect acting on the seed microbiome both pre-and post-dispersal is whether the reduction in secondary metabolites often observed in seeds of domesticated crops 79,80 , along with other changes in seed chemistry influences seed microbiome composition and viability. As many plant pathogenic microorganisms are transmitted via seed, it will be particularly important in future studies to investigate whether changes in seed properties associated with domestication positively or negatively affect the ability of specific microorganisms to survive the dispersal stage and be transmitted to the emerging seedling, or even to transition along the freeliving/parasite/mutualist continuum 81 .…”

Section: The Seed Provides An Ideal Context In Which To Study the Effect Of Plant Domestication On Plant Microbiomesmentioning

confidence: 99%

The effect of plant domestication on host control of the microbiota

et al. 2021

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Macroorganisms are colonized by microbial communities that exert important biological and ecological functions, the composition of which is subject to host control and has therefore been described as “an ecosystem on a leash”. However, domesticated organisms such as crop plants are subject to both artificial selection and natural selection exerted by the agricultural ecosystem. Here, we propose a framework for understanding how host control of the microbiota is influenced by domestication, in which a double leash acts from domesticator to host and host to microbes. We discuss how this framework applies to a plant compartment that has demonstrated remarkable phenotypic changes during domestication: the seed.

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Section: The Seed Provides An Ideal Context In Which To Study the Effect Of Plant Domestication On Plant Microbiomesmentioning

confidence: 99%

The effect of plant domestication on host control of the microbiota

et al. 2021

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“…Since symbiotic fungi have recently been observed in various hemipteran lineages, researchers continually ask themselves about the origin of these associations [14,20,34,35,40]. The literature data indicate three possible evolutionary scenarios: (1) symbiotic fungi may derive from entomopathogenic fungi; (2) they may be the descendants of nonpathogenic commensals; or (3) the ancestor of fungal symbionts may be phytopathogenic fungi [21,35,38]. Most hemipterans are plant sap-sucking insects, and due to their mode of feeding, they are also vectors of plant pathogens.…”

Section: Discussionmentioning

confidence: 99%

“…For this reason, entomopathogenic fungi have also been tested as biological control agents for whiteflies, lepidopterans and scale insects [18,19]. The finding of a close relationship between fungal entomopathogens and symbionts has led to the hypothesis that during their co-evolution, the interaction between both of these partners shifted from parasitism to mutualism [20,21].…”

Section: Introductionmentioning

confidence: 99%

Fungal Associates of Soft Scale Insects (Coccomorpha: Coccidae)

Szklarzewicz

Michalik

Grzywacz

et al. 2021

Cells

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Ophiocordyceps fungi are commonly known as virulent, specialized entomopathogens; however, recent studies indicate that fungi belonging to the Ophiocordycypitaceae family may also reside in symbiotic interaction with their host insect. In this paper, we demonstrate that Ophiocordyceps fungi may be obligatory symbionts of sap-sucking hemipterans. We investigated the symbiotic systems of eight Polish species of scale insects of Coccidae family: Parthenolecanium corni, Parthenolecanium fletcheri, Parthenolecanium pomeranicum, Psilococcus ruber, Sphaerolecanium prunasti, Eriopeltis festucae, Lecanopsis formicarum and Eulecanium tiliae. Our histological, ultrastructural and molecular analyses showed that all these species host fungal symbionts in the fat body cells. Analyses of ITS2 and Beta-tubulin gene sequences, as well as fluorescence in situ hybridization, confirmed that they should all be classified to the genus Ophiocordyceps. The essential role of the fungal symbionts observed in the biology of the soft scale insects examined was confirmed by their transovarial transmission between generations. In this paper, the consecutive stages of fungal symbiont transmission were analyzed under TEM for the first time.

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“…Microbial symbionts can shape host evolution in a diversity of ways (Brucker & Bordenstein, 2012, 2013Gould et al, 2018;Shapira, 2016;Sharon et al, 2010). The extent to which the strength and outcomes of selection could be impacted when symbionts transition along the mutualist-parasite continuum is unclear (Drew et al, 2021). The global distribution of Leucobacter among plants, animals and free-living environments demonstrates extraordinary niche diversity indicative of a generalist.…”

Section: Discussionmentioning

confidence: 99%

A globally ubiquitous symbiont can drive experimental host evolution

2021

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Organisms harbour myriad microbes which can be parasitic or protective against harm.The costs and benefits resulting from these symbiotic relationships can be contextdependent, but the evolutionary consequences to hosts of these transitions remain unclear. Here, we mapped the Leucobacter genus across 13,715 microbiome samples (163 studies) to reveal a global distribution as a free-living microbe or a symbiont of animals and plants. We showed that across geographically distant locations (South Africa, France, Cape Verde), Leucobacter isolates vary substantially in their virulence to an associated animal host, Caenorhabditis nematodes. We further found that multiple Leucobacter sequence variants co-occur in wild Caenorhabditis spp. which combined with natural variation in virulence provides real-world potential for Leucobacter community composition to influence host fitness. We examined this by competing C. elegans genotypes that differed in susceptibility to different Leucobacter species in an evolution experiment. One Leucobacter species was found to be host-protective against another, virulent parasitic species. We tested the impact of host genetic background and Leucobacter community composition on patterns of host-based defence evolution. We found host genotypes conferring defence against the parasitic species were maintained during infection. However, when hosts were protected during coinfection, host-based defences were nearly lost from the population. Overall, our results provide insight into the role of community context in shaping host evolution during symbioses.

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Microbial evolution and transitions along the parasite–mutualist continuum

Cited by 207 publications

References 255 publications

The effect of plant domestication on host control of the microbiota

The effect of plant domestication on host control of the microbiota

Fungal Associates of Soft Scale Insects (Coccomorpha: Coccidae)

A globally ubiquitous symbiont can drive experimental host evolution

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