Exchange of Microbiomes in Plant-Insect Herbivore Interactions

Pirttilä, Anna Maria; Brusila, Veera; Koskimäki, Janne J.; Wäli, Piippa R.; Ruotsalainen, Anna Liisa; Mutanen, Marko; Markkola, Anna Mari

doi:10.1128/mbio.03210-22

Cited by 19 publications

(14 citation statements)

References 137 publications

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“…Our study also reveals beetle-mediated alterations in wood bacterial assemblage, similar to insect herbivores that reshape the native plant leaf microbiome (92). However, the degree of overlap or distinctiveness between insect and host (wood) microbiome remains ambiguous (93). Precisely, higher sharing between fed wood and beetle samples followed by higher bacterial diversity in fed wood samples than in control wood can be due to several reasons.…”

Section: Discussionmentioning

confidence: 99%

Comparative metagenomic study unveils bacterial communities and their putative involvement in ecological success of two pine-feedingIpsbeetle holobionts

Khara,

Chakraborty,

Modlinger

et al. 2024

Preprint

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Climate change has recently boosted the severity and frequency of the pine bark beetle attacks. The bacterial community associated with these beetles acts as “hidden players”, enhancing their ability to infest and thrive on defence-rich pine trees. There is limited understanding of the environmental acquisition of these hidden players and their life stage-specific association with different pine-feeding bark beetles. There is inadequate knowledge on novel bacterial introduction to pine trees after the beetle infestation. Hence, we conducted the first comparative bacterial metabarcoding study comprehensively revealing the bacterial communities in the pine trees before and after beetle feeding and in different life stages of two dominant pine-feeding bark beetles, namelyIps sexdentatusandIps acuminatus. We also evaluated the bacterial association between wild and lab-bred beetles to measure the deviation due to inhabiting a controlled environment. Significant differences in bacterial amplicon sequence variance (ASVs) abundance existed among different life stages within and between the pine beetles. Such observations endorsed that the bark beetle life stage shaped bacterial assemblage. Furthermore, lab-bred and wild-collected adult beetles had distinct bacterial assemblages, implying that the breeding environment induced crucial changes. Alteration of pine wood bacteriome after beetle feeding is an intriguing observation in the present study, which demands further investigation. We validated the relative abundances of selected bacterial taxa estimated by metagenomic sequencing with quantitative PCR. Functional predictions revealed that these bacterial genera might execute conserved functions, aiding the ecological success of these beetles. Nevertheless, these findings shed new insights into bacterial associations and their putative metabolic roles in pine beetles under the influence of various drivers such as environment, host, and life stages and provide the foundation for future downstream functional investigations.ImportanceThe current understanding of bark beetle as holobiont is restricted. Most studies lack information on microbial community assembly in bark beetle microhabitats. No data comprehensively reveals the influence of lab breeding on pine beetle microbial associations. It is unknown if there is any adaptive convergence in beetle microbial assemblage due to feeding on the same host. Such information is essential to developing a bark beetle management strategy to restore forests from beetle-mediated damage. Our study shows that lab-breeding considerably influences beetle bacterial community assembly. We documented that beetle feeding alters bacteriome at the microhabitat level, and the beetle life stage shapes the bacterial associations. Nevertheless, our study revisited the bark beetle symbiosis under the influence of different drivers and revealed intriguing insight into bacterial community assembly, facilitating future functional studies.

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Section: Discussionmentioning

confidence: 99%

Comparative metagenomic study unveils bacterial communities and their putative involvement in ecological success of two pine-feedingIpsbeetle holobionts

Khara,

Chakraborty,

Modlinger

et al. 2024

Preprint

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“…First , Weissella bacteria may initially infect plant seeds and subsequently colonize silverfish and ant guts upon feeding. Studies have shown that the microbiotic communities of insect herbivores can be contingent on the microbiome of the host plant (Chung et al, 2017; Mogouong et al, 2021; Pirttilä et al, 2023; Strano et al, 2018). For our focal system, this scenario implies that Weissella acquisition is likely associated with the granivorous feeding behaviour of Messor -specialized Neoasterolepisma.…”

Section: Discussionmentioning

confidence: 99%

Co-habiting ants and silverfish display a converging feeding ecology

Parmentier,

Molero-Baltanás,

Valdivia

et al. 2023

Preprint

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Species from a great number of animal taxa have specialized to living with social hosts. Depending on their level of specialization, these symbiotic animals are characterized by distinct behavioural, chemical, and morphological traits that enable close heterospecific interactions. Despite its functional importance, our understanding of the feeding ecology of specialized animals living with social hosts remains limited.In this study, we examined how host specialization of silverfish co-habiting with ants affects several components of their feeding ecology. We combined stable isotope profiling, feeding assays, phylogenetic reconstruction, and microbial community characterization of theNeoasterolepismasilverfish genus and a wider nicoletiid and lepismatid silverfish panel where divergent myrmecophilous lifestyles are observed.Stable isotope profiling (δ13C and δ15N) showed that the isotopic niches (proxy for trophic niches) of granivorousMessorants andMessor-specializedNeoasterolepismaexhibit a remarkable overlap within an ant nest. Trophic experiments and gut dissections further supported that these specializedNeoasterolepismasilverfish transitioned to a diet that includes plant seeds. In contrast, the isotopic niches of generalistNeoasterolepismasilverfish and generalist nicoletiid silverfish were clearly different from their ant hosts within the shared nest environment.The impact of the myrmecophilous lifestyle on feeding ecology was also evident in the internal silverfish microbiome. Compared to generalists,Messor-specialists exhibited a higher bacterial density and a higher proportion of heterofermentative lactic acid bacteria. Moreover, the nest environment explained the infection profile (or the 16S rRNA genotypes) ofWeissellabacteria inMessor-specialized silverfish and the ant hosts.Together, we show that social hosts are important determinants for the feeding ecology of symbiotic animals, and can induce diet convergence.

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“…For instance, soil microorganisms can influence plant metabolism through their direct interaction with the host or, indirectly, by improving the availability of resources 9 . This, in turn, can alter the composition of aboveground plant tissue and directly influence the herbivore microbiome (e.g., changes in diet 10 ) and indirectly (e.g., changes in leaf microbiome and consequent changes in a potential source of the herbivore microbiome 11 ). In addition, soil microorganisms can become endophytes of plants and move from soil to aboveground tissue via the xylem 12 .…”

Section: Introductionmentioning

confidence: 99%

Soil microbiota and herbivory drive the assembly of tomato plant-associated microbial communities through different mechanisms

Malacrinò,

Bennett

2024

Commun Biol

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Plant-associated microbial communities are key to shaping many aspects of plant biology. In this study, we tested whether soil microbial communities and herbivory influence the bacterial community of tomato plants and whether their influence in different plant compartments is driven by microbial spillover between compartments or whether plants are involved in mediating this effect. We grew our plants in soils hosting three different microbial communities and covered (or not) the soil surface to prevent (or allow) passive microbial spillover between compartments, and we exposed them (or not) to herbivory by Manduca sexta. Here we show that the soil-driven effect on aboveground compartments is consistently detected regardless of soil coverage, whereas soil cover influences the herbivore-driven effect on belowground microbiota. Together, our results suggest that the soil microbiota influences aboveground plant and insect microbial communities via changes in plant metabolism and physiology or by sharing microorganisms via xylem sap. In contrast, herbivores influence the belowground plant microbiota via a combination of microbial spillover and changes in plant metabolism. These results demonstrate the important role of plants in linking aboveground and belowground microbiota, and can foster further research on soil microbiota manipulation for sustainable pest management.

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Exchange of Microbiomes in Plant-Insect Herbivore Interactions

Abstract: Prokaryotic and eukaryotic microbial symbiotic communities span through kingdoms. The vast microbial gene pool extends the host genome and supports adaptations to changing environmental conditions.

Cited by 19 publications

References 137 publications

Comparative metagenomic study unveils bacterial communities and their putative involvement in ecological success of two pine-feedingIpsbeetle holobionts

Comparative metagenomic study unveils bacterial communities and their putative involvement in ecological success of two pine-feedingIpsbeetle holobionts

Co-habiting ants and silverfish display a converging feeding ecology

Soil microbiota and herbivory drive the assembly of tomato plant-associated microbial communities through different mechanisms

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