Competition-based screening secures the evolutionary stability of a defensive microbiome

Sf, Worsley; Tm, Innocent; Na, Holmes; Mm, Al-Bassam; Wilkinson, Barrie; Jc, Murrell; Boomsma, JJ; Yu, Douglas W.; Hutchings, Matthew I.

doi:10.1101/2020.11.24.395384

Cited by 3 publications

(4 citation statements)

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“…R markdown-format scripts, input datafiles, and html output files for the analyses in the main text Figures 4, 5, and 6 and in Figures S9 and S10 (Additional File 1) are provided as a single R project folder at github.com/ dougwyu/Worsley_et_al_screening_test_R_code [99]…”

Section: Statistical Analysesmentioning

confidence: 99%

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Competition-based screening helps to secure the evolutionary stability of a defensive microbiome

et al. 2021

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Background The cuticular microbiomes of Acromyrmex leaf-cutting ants pose a conundrum in microbiome biology because they are freely colonisable, and yet the prevalence of the vertically transmitted bacteria Pseudonocardia, which contributes to the control of Escovopsis fungus garden disease, is never compromised by the secondary acquisition of other bacterial strains. Game theory suggests that competition-based screening can allow the selective recruitment of antibiotic-producing bacteria from the environment, by providing abundant resources to foment interference competition between bacterial species and by using Pseudonocardia to bias the outcome of competition in favour of antibiotic producers. Results Here, we use RNA-stable isotope probing (RNA-SIP) to confirm that Acromyrmex ants can maintain a range of microbial symbionts on their cuticle by supplying public resources. We then used RNA sequencing, bioassays, and competition experiments to show that vertically transmitted Pseudonocardia strains produce antibacterials that differentially reduce the growth rates of other microbes, ultimately biassing the bacterial competition to allow the selective establishment of secondary antibiotic-producing strains while excluding non-antibiotic-producing strains that would parasitise the symbiosis. Conclusions Our findings are consistent with the hypothesis that competition-based screening is a plausible mechanism for maintaining the integrity of the co-adapted mutualism between the leaf-cutting ant farming symbiosis and its defensive microbiome. Our results have broader implications for explaining the stability of other complex symbioses involving horizontal acquisition.

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Section: Statistical Analysesmentioning

confidence: 99%

“…4, 5, and 6 and in Additional file 1: Fig. S8 & S9 are also provided as a single R project folder at github.com/dougwyu/Worsley_et_al_screening_test_R_code [99].…”

Section: Availability Of Data and Materialsmentioning

confidence: 99%

Competition-based screening helps to secure the evolutionary stability of a defensive microbiome

et al. 2021

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“…But a range of insects acquire symbionts from the environment, retaining a subset of the inoculated microbes [17][18][19][20] due to their physiology and behavior [21,22], or to competitive actions of their regular symbiont partners ( e.g. Worsley et al [23]; Itoh et al [24]). Among the diverse range of hexapods with environmental symbiont acquisition, some have evolved highly selective partner choice mechanisms, retaining a specific, beneficial subset of their starting inoculum due to anatomical and physiological innovations [25,26].…”

Section: Introductionmentioning

confidence: 99%

The secrets to domestic bliss – Partner fidelity and environmental filtering preserve stage-specific turtle ant gut symbioses for over 40 million years

D’Amelio

Béchade

et al. 2021

Preprint

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Background: Gut microbiomes can vary across development, a pattern often found for insects with complete metamorphosis. With varying nutritional need and distinct opportunities for microbial acquisition, questions arise as to how such holometabolous insects retain helpful microbes at larval and adult stages. Ants are an intriguing system for such study. In a number of lineages adults digest only liquid food sources, while larvae digest solid foods. Like some other social insects, workers and soldiers of some ant species engage in oral-anal trophallaxes, enabling microbial transfer among siblings. But do queens, the typical colony founding caste, obtain symbionts through such transfer? Does this enable transgenerational symbiont passage? And does the resulting partner fidelity promote the evolution of beneficial symbionts? Furthermore, how might such adult-centric biology shape larval microbiomes? To address these questions, we characterized symbiotic gut bacteria across 13 species of Cephalotes turtle ants, with up to 40-million years of divergence. Adding to the prior focus on workers we, here, study underexplored castes and stages including queens, soldiers, and larvae, by performing 16S rRNA qPCR, amplicon sequencing, and phylogenetic classification. Results: We show that adult microbiomes are conserved across species and largely across castes. Nearly 95% of the bacteria in adults have, thus far, been found only in Cephalotes ants. Furthermore, the microbiomes from most adults exhibit phylosymbiosis, a trend in which microbiome community similarity recapitulates patterns of host relatedness. Additionally, an abundant, adult-enriched symbiont cospeciates with some Cephalotes. Evidence here suggests that these partner fidelity patterns extend from transgenerational symbiont transfer through alate gyne dispersal and subsequent colony-founding by queens. Like adults, larvae of Cephalotes species exhibit strong microbiome conservation. Phylosymbiosis patterns are weaker, however, with further evidence elevating environmental filtering as a primary mechanism behind such conservation. Specifically, while adult-enriched symbionts are found in most larvae, symbionts of older larvae are highly related to free-living bacteria from the Enterobacteriaceae, Lactobacillales, and Actinobacteria. Conclusions: Our findings suggest that both partner fidelity and conserved environmental filtering drive stable, stage-specific, social insect symbioses. We discuss the implications for our broader understanding of insect microbiomes, and the means of sustaining a beneficial microbiome.

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“…But a range of insects acquire symbionts from the environment, retaining a subset of the inoculated microbes [17][18][19][20] due to their physiology and behavior [21,22], or to competitive actions of their regular symbiont partners ( e.g. Worsley et al [23]; Itoh et al [24]). Among the diverse range of hexapods with environmental symbiont acquisition, some have evolved highly selective partner choice mechanisms, retaining a speci c, bene cial subset of their starting inoculum due to anatomical and physiological innovations [25,26].…”

Section: Introductionmentioning

confidence: 99%

The Secrets to Domestic Bliss – Partner Fidelity and Environmental Filtering Preserve Stage-Specific Turtle Ant Gut Symbioses for Over 40 Million Years

D’Amelio

Béchade

et al. 2021

Preprint

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BackgroundGut microbiomes can vary across development, a pattern often found for insects with complete metamorphosis. With varying nutritional need and distinct opportunities for microbial acquisition, questions arise as to how such ‘holometabolous’ insects retain helpful microbes at larval and adult stages. Ants are an intriguing system for such study. In a number of lineages adults digest only liquid food sources, while larvae digest solid foods. Like some other social insects, workers and soldiers of some ant species engage in oral-anal trophallaxes, enabling microbial transfer among siblings. But do queens, the typical colony founding caste, obtain symbionts through such transfer? Does this enable transgenerational symbiont passage? And does the resulting partner fidelity promote the evolution of beneficial symbionts? Furthermore, how might such adult-centric biology shape larval microbiomes? To address these questions, we characterized symbiotic gut bacteria across 13 species of Cephalotes turtle ants, with up to 40-million years of divergence. Adding to the prior focus on workers we, here, study underexplored castes and stages including queens, soldiers, and larvae, by performing 16S rRNA qPCR, amplicon sequencing, and phylogenetic classification. ResultsWe show that adult microbiomes are conserved across species and largely across castes. Nearly 95% of the bacteria in adults have, thus far, been found only in Cephalotes ants. Furthermore, the microbiomes from most adults exhibit phylosymbiosis, a trend in which microbiome community similarity recapitulates patterns of host relatedness. Additionally, an abundant, adult-enriched symbiont cospeciates with some Cephalotes. Evidence here suggests that these partner fidelity patterns extend from transgenerational symbiont transfer through alate gyne dispersal and subsequent colony-founding by queens. Like adults, larvae of Cephalotes species exhibit strong microbiome conservation. Phylosymbiosis patterns are weaker, however, with further evidence elevating environmental filtering as a primary mechanism behind such conservation. Specifically, while adult-enriched symbionts are found in most larvae, symbionts of older larvae are highly related to free-living bacteria from the Enterobacteriaceae, Lactobacillales, and Actinobacteria. ConclusionsOur findings suggest that both partner fidelity and conserved environmental filtering drive stable, stage-specific, social insect symbioses. We discuss the implications for our broader understanding of insect microbiomes, and the means of sustaining a beneficial microbiome.

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Competition-based screening secures the evolutionary stability of a defensive microbiome

Cited by 3 publications

References 84 publications

Competition-based screening helps to secure the evolutionary stability of a defensive microbiome

Competition-based screening helps to secure the evolutionary stability of a defensive microbiome

The secrets to domestic bliss – Partner fidelity and environmental filtering preserve stage-specific turtle ant gut symbioses for over 40 million years

The Secrets to Domestic Bliss – Partner Fidelity and Environmental Filtering Preserve Stage-Specific Turtle Ant Gut Symbioses for Over 40 Million Years

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