Crosstalk between the microbiota and insect postembryonic development

Girard, Maxime; Luis, Patricia; Moro, Claire Valiente; Minard, Guillaume

doi:10.1016/j.tim.2022.08.013

Cited by 17 publications

(17 citation statements)

References 115 publications

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“…As an example, dragonflies change their microbiome richness when they change from aquatic life in larval stages to terrestrial life in their adulthood [ 19 ]. A recent review summarised that the insect gut hosts the highest diversity of microbes across all invertebrates [ 7 ], providing a high potential for intraspecific variation. Guts shape microbial communities via chemical and physical conditions such as pH, nutrient availability, immune system, oxygen levels, and compartmentalisation.…”

Section: Key Drivers Of Intraspecific Variation In Microbial Communitiesmentioning

confidence: 99%

“…Current challenges in microbiome research are to go beyond descriptive studies towards functional analysis at lower taxonomic levels (within phyla, families, genera, and species) of microbe-microbe and microbe-host interactions, community effects and the targeted manipulation of microbiomes [ 1 , 7 , 8 ]. This requires measuring and modelling the resilience of host-associated microbial communities in non-model species in the field to generate quantifiable data [ 11 , 134 , 135 ].…”

Section: Outstanding Questions and Future Research Directionsmentioning

confidence: 99%

“…Host species and diet/trophy appear to be the most relevant drivers, but sex, life stage, and sample origin/habitat also have some impact, while the abundance of endosymbionts and phylogeny only have weak influence [ 2 – 6 ]. Intraspecific microbiome variation can be driven by several factors, such as the host itself, the diet, and the environment [ 7 – 9 ]. Microbe transmission routes, recruitment, maintenance, and interactions further shape these variations [ 10 – 12 ].…”

Section: Introductionmentioning

confidence: 99%

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Impact of intraspecific variation in insect microbiomes on host phenotype and evolution

Lange,

Boyer,

Bezemer

et al. 2023

The ISME Journal

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Microbes can be an important source of phenotypic plasticity in insects. Insect physiology, behaviour, and ecology are influenced by individual variation in the microbial communities held within the insect gut, reproductive organs, bacteriome, and other tissues. It is becoming increasingly clear how important the insect microbiome is for insect fitness, expansion into novel ecological niches, and novel environments. These investigations have garnered heightened interest recently, yet a comprehensive understanding of how intraspecific variation in the assembly and function of these insect-associated microbial communities can shape the plasticity of insects is still lacking. Most research focuses on the core microbiome associated with a species of interest and ignores intraspecific variation. We argue that microbiome variation among insects can be an important driver of evolution, and we provide examples showing how such variation can influence fitness and health of insects, insect invasions, their persistence in new environments, and their responses to global environmental changes.

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Section: Key Drivers Of Intraspecific Variation In Microbial Communitiesmentioning

confidence: 99%

Section: Outstanding Questions and Future Research Directionsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Impact of intraspecific variation in insect microbiomes on host phenotype and evolution

Lange,

Boyer,

Bezemer

et al. 2023

The ISME Journal

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“…While our current understanding of the consequences of moulting and maternal care on the dynamics of the host microbiome during development is mainly based on holometabolous insects, little is known about these consequences on hemimetabolous species (Hammer and Moran, 2019; Girard et al ., 2023). The focus on holometabolous species is explained by the fact that their immature stages have a morphology and sometimes an ecology very different from those of adults, which raises obvious questions about the fate of their microbiome during metamorphosis (Johnston et al ., 2019).…”

Section: Introductionmentioning

confidence: 99%

Microbiome turnover during offspring development varies with maternal care, but not moult, in a hemimetabolous insect

Cheutin,

Boucicot,

Meunier

2024

Preprint

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The ecological success of insects often depends on their association with beneficial microbes. However, insect development involves repeated moults, which can have dramatic effects on their microbial communities. Here, we investigated whether and how moulting affects the microbiome of a hemimetabolous insect, and whether maternal care can modulate these effects. We reared European earwig juveniles with or without mothers and used 16S rRNA metabarcoding to analyse the whole microbiome of eggs, recently and old moulted individuals at four developmental stages and the resulting adults. The 218 samples obtained showed that the microbiome diversity changed non-linearly during development and that these changes were associated with bacterial biomarkers. Surprisingly, these changes did not occur during moulting, but rather between the beginning and end of certain developmental stages. We also found that access to maternal care affected the microbiome of both juveniles and adults, even when the last contact with mothers was two months before adulthood. Overall, these results provide new insights into our understanding of the (in)stability of the microbiome in hemimetabolous insects and its independence from moult. More generally, they question the role of microbiome acquisition through maternal care in maintaining family life in species where this behaviour is facultative.

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“…Hammer and Bowe claimed the "gut microbial facilitation hypothesis" explained that the adaptability of phytophagous pests to parasitic plants is related to the gut microbiota variation (Hammer and Bowers, 2015;Girard et al, 2022). Over millions of years of evolution, insects and gut microbes have coevolved, interacted, and cooperated into an inseparable symbiotic correlation (Hammer and Bowers, 2015).…”

Section: Introductionmentioning

confidence: 99%

Gut microbiota contributes to lignocellulose deconstruction and nitrogen fixation of the larva of Apriona swainsoni

Zhang

Tian²,

Hu³

et al. 2022

Front. Physiol.

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Apriona swainsoni is a vital forest pest prevalent in China. The larvae of A. swainsoni live solely in the branches of trees and rely entirely on the xylem for nutrition. However, there is still a lack of in-depth research on the gut microbiota’s use of almost nitrogen-free wood components to provide bio-organic macromolecular components needed for their growth. Thus, in this study, the metagenome, metaproteome, and metabolome of the A. swainsoni larvae in four gut segments (foregut; midgut; anterior hindgut; posterior hindgut) were analyzed by the multi-omics combined technology, to explore the metabolic utilization mechanism of the corresponding gut microbiota of A. swainsoni. Firstly, we found that the metagenome of different gut segments was not significantly different in general, but there were different combinations of dominant bacteria and genes in different gut segments, and the metaproteome and metabolome of four gut segments were significantly different in general. Secondly, the multi-omics results showed that there were significant gradient differences in the contents of cellulose and hemicellulose in different segments of A. swainsoni, and the expression of corresponding metabolic proteins was the highest in the midgut, suggesting the metabolic characteristics of these lignocellulose components in A. swainsoni gut segments. Finally, we found that the C/N ratio of woody food was significantly lower than that of frass, and metagenomic results showed that nitrogen fixation genes mainly existed in the foregut and two hindgut segments. The expression of the key nitrogen fixing gene nifH occurred in two hindgut parts, indicating the feature of nitrogen fixation of A. swainsoni. In conclusion, our results provide direct evidence that the larvae of A. swainsoni can adapt to the relatively harsh niche conditions through the highly organized gut microbiome in four gut segments, and may play a major role in their growth.

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Crosstalk between the microbiota and insect postembryonic development

Cited by 17 publications

References 115 publications

Impact of intraspecific variation in insect microbiomes on host phenotype and evolution

Impact of intraspecific variation in insect microbiomes on host phenotype and evolution

Microbiome turnover during offspring development varies with maternal care, but not moult, in a hemimetabolous insect

Gut microbiota contributes to lignocellulose deconstruction and nitrogen fixation of the larva of Apriona swainsoni

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