Specialized acquisition behaviors maintain reliable environmental transmission in an insect-microbial mutualism

Villa, Scott M.; Chen, Jason Z.; Kwong, Zeeyong; Acosta, Alice; Vega, Nicole M.; Gerardo, Nicole M.

doi:10.1016/j.cub.2023.05.062

Cited by 14 publications

(10 citation statements)

References 84 publications

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“…We inoculated second instar squash bug nymphs with approximately 1:1 mixtures of GA-OX1 sfGFP with GA-OX1 RFP, diluted to produce inocula ranging from approximately 10 6 to 10 1 CFU/μL ( S1A Fig ). These inoculum densities are within the natural range of variation in symbiont density that hosts might encounter, whether in freshly deposited adult feces (10 5 to 5 × 10 6 CFUs/μL), on which nymphs can feed to acquire symbionts [ 37 ], or in soil, in which Caballeronia is present at lower densities alongside many other microbes [ 38 , 39 ].…”

Section: Resultsmentioning

confidence: 99%

Ecological drift during colonization drives within-host and between-host heterogeneity in an animal-associated symbiont

Chen,

Kwong,

Gerardo

et al. 2024

PLoS Biol

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Specialized host–microbe symbioses canonically show greater diversity than expected from simple models, both at the population level and within individual hosts. To understand how this heterogeneity arises, we utilize the squash bug, Anasa tristis, and its bacterial symbionts in the genus Caballeronia. We modulate symbiont bottleneck size and inoculum composition during colonization to demonstrate the significance of ecological drift, the noisy fluctuations in community composition due to demographic stochasticity. Consistent with predictions from the neutral theory of biodiversity, we found that ecological drift alone can account for heterogeneity in symbiont community composition between hosts, even when 2 strains are nearly genetically identical. When acting on competing strains, ecological drift can maintain symbiont genetic diversity among different hosts by stochastically determining the dominant strain within each host. Finally, ecological drift mediates heterogeneity in isogenic symbiont populations even within a single host, along a consistent gradient running the anterior-posterior axis of the symbiotic organ. Our results demonstrate that symbiont population structure across scales does not necessarily require host-mediated selection, as it can emerge as a result of ecological drift acting on both isogenic and unrelated competitors. Our findings illuminate the processes that might affect symbiont transmission, coinfection, and population structure in nature, which can drive the evolution of host–microbe symbioses and microbe–microbe interactions within host-associated microbiomes.

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Section: Resultsmentioning

confidence: 99%

Ecological drift during colonization drives within-host and between-host heterogeneity in an animal-associated symbiont

Chen,

Kwong,

Gerardo

et al. 2024

PLoS Biol

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“…We found upregulation of metabolic processes in the bodies of symbiotic insects relative to the bodies of aposymbiotic insects. This relative increase in metabolism may reflect the fact that symbiotic A. tristis dedicate more time to feeding than aposymbiotic insects (Villa et al, 2023) and grow more rapidly (Acevedo et al, 2021), requiring more energy to sustain their rapid development. We further found several biosynthetic processes upregulated in the symbiotic crypts relative to the aposymbiotic crypts.…”

Section: Discussionmentioning

confidence: 99%

Differential gene expression in the insect vector Anasa tristis in response to symbiont colonization but not infection with a vectored phytopathogen

Mendiola,

Chen,

Lukubye

et al. 2024

Front. Ecol. Evol.

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Many insects selectively associate with specific microbes in long-term, symbiotic relationships. Maintaining these associations can be vital for the insect hosts’ development, but insects must also contend with potential coinfections from other microbes in the environment. Fending off microbial threats while maintaining mutualistic microbes has resulted in many insects developing specialized symbiotic organs to house beneficial microbes. Though locally concentrated in these organs, symbiont establishment can have global consequences for the insect, including influence over the success of coinfecting microbes in colonizing the insect host. We use a transcriptomic approach to examine how the mutualistic symbiosis between the agricultural pest Anasa tristis and bacteria in the genus Caballeronia affects insect gene expression locally within the symbiotic organs and in the insect host at large. We simultaneously determine whether Caballeronia colonization impacts insect host responses to infection with the plant pathogen Serratia marcescens, which it vectors to plants. We found that no significant differential gene expression was elicited by infection with S. marcescens. This was a surprising finding given previous work indicating that symbiotic A. tristis clear S. marcescens infection rapidly compared to aposymbiotic individuals. Our results indicate that symbiotic and nonsymbiotic tissues in A. tristis differ greatly in their gene expression, particularly following successful symbiont colonization. We found evidence for local downregulation of host immunity and upregulation of cell communication within the symbiotic organs, functions which can facilitate the success of the A. tristis-Caballeronia symbiosis.

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“…Although we implemented our experiments using horizontal transmission, many symbioses exhibit elaborate, host-controlled mechanisms that ensure vertical transmission from parent to offspring [2,[44][45][46][47], including even our own model system [48]. We argue that vertical transmission strategies are not immune to the effects of ecological drift, which acts on communities regardless of how they disperse.…”

Section: Discussionmentioning

confidence: 99%

Ecological drift during colonization drives within- and between-host heterogeneity in animal symbiont populations

Chen,

Kwong,

Gerardo

et al. 2023

Preprint

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Host-associated microbiomes vary greatly in composition both within and between host individuals, providing the raw material for natural selection to act on host-microbe associations. Nonetheless, the drivers of compositional heterogeneity in host-associated microbiomes have only rarely been examined. To understand how this heterogeneity arises, we utilize the squash bug,Anasa tristis, and its bacterial symbionts in the genusCaballeronia. We artificially modulate symbiont bottleneck size and strain diversity during colonization to demonstrate the significance of ecological drift, which causes stochastic fluctuations in community composition. Consistent with predictions from the neutral theory of biodiversity, ecological drift alone can account for heterogeneity in symbiont community composition between hosts, even when two strains are nearly genetically identical. When acting on competing, unrelated strains, ecological drift can maintain symbiont genetic diversity among different hosts by stochastically determining the dominant strain within each host. Finally, ecological drift mediates heterogeneity in isogenic symbiont populations even within a single host, along a consistent gradient running the anterior-posterior axis of the symbiotic organ. Our results demonstrate that symbiont population structure across scales does not necessarily require host-mediated selection, but emerges as a result of ecological drift acting on both isogenic and unrelated competitors. Our findings illuminate the processes that might affect symbiont transmission, coinfection, and population structure in nature, which can drive the evolution of host-microbe symbiosis and microbe-microbe interactions within host-associated microbiomes.

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Specialized acquisition behaviors maintain reliable environmental transmission in an insect-microbial mutualism

Cited by 14 publications

References 84 publications

Ecological drift during colonization drives within-host and between-host heterogeneity in an animal-associated symbiont

Ecological drift during colonization drives within-host and between-host heterogeneity in an animal-associated symbiont

Differential gene expression in the insect vector Anasa tristis in response to symbiont colonization but not infection with a vectored phytopathogen

Ecological drift during colonization drives within- and between-host heterogeneity in animal symbiont populations

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