Seasonal Shifts in Bacterial and Fungal Microbiomes of Leaves and Associated Leaf-Mining Larvae Reveal Persistence of Core Taxa Regardless of Diet

Šigutová, Hana; Šigut, Martin; Pyszko, Petr; Kostovčík, Martin; Kolařík, Miroslav; Drozd, Pavel

doi:10.1128/spectrum.03160-22

Cited by 13 publications

(16 citation statements)

References 118 publications

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“…Alpha diversity indices of epiphytic bacteria and fungi in this study showed significant differences among all five plant species. Šigutová et al. (2023) demonstrated that the diversity of bacteria was significantly impacted by the species of the host plant, whereas the composition of the fungal community was more strongly influenced by the host species.…”

Section: Discussionmentioning

confidence: 99%

“…Šigutová et al. ( Šigutová et al., 2023 ) conducted a study to investigate the impact of season on the composition of epiphytic bacterial communities. The results revealed that there were significant variations in the bacterial communities between different months, with the most pronounced differences observed between April and the other months.…”

Section: Discussionmentioning

confidence: 99%

“…(1993) demonstrated that the diversity of the epiphytic fungal community in the phyllosphere of Beta vulgaris was lower in spring compared to autumn. The variation in leaf characteristics and environmental factors between young and old leaves, along with the influence of host plant species, play crucial roles in shaping leaf-associated communities and account for the observed differences ( Šigutová et al., 2023 ). Overall, our study provides confirmation of significant seasonal fluctuations in the composition of phyllosphere epiphytic bacteria and fungi ( Jumpponen and Jones, 2010 ; Gomes et al., 2018 ; Postiglione et al., 2022 ).…”

Section: Discussionmentioning

confidence: 99%

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Seasonal dynamics of phyllosphere epiphytic microbial communities of medicinal plants in farmland environment

He,

Zhang,

et al. 2024

Front. Plant Sci.

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IntroductionThe phyllosphere of plants is inhabited by various microorganisms, which play a crucial role in plant physiological metabolism. Currently, there is limited research on the dynamic effects of species and seasons on plant phyllosphere microbial community diversity and microbial interactions.MethodsIn this study, high-throughput sequencing technology was used to sequence the leaf surface parasitic microorganisms of five medicinal plants (Bupleurum chinense, Atractylodes lancea, Salvia miltiorrhiza, Astragalus membranaceus, and Lonicera japonica).ResultsThe results showed that bacteria and fungi clustered into 3,898 and 1,572 operational taxonomic units (OTUs), respectively. Compared to host species, seasons had a more significant impact on the a diversity of bacteria and fungi. The heterogeneity of phyllosphere microbial communities was greater in winter compared to summer. Key species analysis at the OTU level and Spearman correlation analysis demonstrated significant preferences in microbial interactions under plant and seasonal backgrounds. The network connections between bacterial and fungal communities significantly increased during seasonal transitions compared to connections with plants.DiscussionThis study enhances our understanding of the composition and ecological roles of plant-associated microbial communities in small-scale agricultural environments. Additionally, it provides valuable insights for assessing the biodiversity of medicinal plants.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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Seasonal dynamics of phyllosphere epiphytic microbial communities of medicinal plants in farmland environment

He,

Zhang,

et al. 2024

Front. Plant Sci.

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“…Recent studies indicate that the acquisition of novel genes from bacteria and fungi could modify the gut microbiome of herbivorous insects, such as miners, in such a way that the spectrum of consumed plant hosts could be significantly changed (Hammer & Bowers, 2015;Giron et al, 2016;McKenna et al, 2019;Sigutov a et al, 2023).…”

Section: The Environmental Context In the Evolution Of Miningmentioning

confidence: 99%

Middle Jurassic insect mines on gymnosperms provide missing links to early mining evolution

Xiao,

Labandeira,

et al. 2024

New Phytologist

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Summary We investigated the mining mode of insect feeding, involving larval consumption of a plant's internal tissues, from the Middle Jurassic (165 million years ago) Daohugou locality of Northeastern China. Documentation of mining from the Jurassic Period is virtually unknown, and results from this time interval would address mining evolution during the temporal gap of mine–seed plant diversifications from the previous Late Triassic to the subsequent Early Cretaceous. Plant fossils were examined with standard microscopic procedures for herbivory and used the standard functional feeding group–damage‐type system of categorizing damage. All fossil mines were photographed and databased. We examined 2014 plant specimens, of which 27 occurrences on 14 specimens resulted in eight, new, mine damage types (DTs) present on six genera of bennettitalean, ginkgoalean, and pinalean gymnosperms. Three conclusions emerge from this study. First, these mid‐Mesozoic mines are morphologically conservative and track plant host anatomical structure rather than plant phylogeny. Second, likely insect fabricators of these mines were three basal lineages of polyphagan beetles, four basal lineages of monotrysian moths, and a basal lineage tenthredinoid sawflies. Third, the nutrition hypothesis, indicating that miners had greater access to nutritious, inner tissues of new plant lineages, best explains mine evolution during the mid‐Mesozoic.

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“…We aimed to (i) investigate the effect of AGM taxonomy on mycobiome diversity and composition; (ii) compare the mycobiome of individual gall compartments and investigate the involvement of neutral processes in fungal community assembly; and (iii) discuss the potential functional significance of the revealed fungal symbionts. We hypothesized that larvae would harbor fungal microbes different from nutritive mycelia, in analogy to detritophagous and herbivorous insects ( 33 , 34 , 43 ). Based on this assumption, presumed symbiosis with B. dothidea, and the active suppression of unsuitable taxa by larval symbionts ( 44 ), we expected a lower involvement of neutral processes in the gall interior and larval microbiome compared to the gall surface.…”

Section: Introductionmentioning

confidence: 99%

Mycobiomes of two distinct clades of ambrosia gall midges (Diptera: Cecidomyiidae) are species-specific in larvae but similar in nutritive mycelia

Pyszko,

Šigutová,

Kolařík

et al. 2024

Microbiol Spectr

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Ambrosia gall midges (AGMs) are mostly host plant-specific. In their galls, they harbor fungal symbionts on which they feed. Therefore, they represent unique steps in the evolution of the gall-forming Cecidomyiidae (Diptera). Gall-associated fungi have been studied predominantly by cultivations, and potential larval endosymbionts have been completely neglected. Using ITS2 rRNA metabarcoding, we characterized the mycobiomes of individual gall compartments (gall surface, gall interior, and larva) of six species from two phylogenetically separated tribes (Asphondyliini and Lasiopterini). Compared to the gall surface and interior, the larvae harbored significantly higher fungal richness and taxonomic diversity, and a larger pool of indicator taxa. Larval mycobiome composition was more species-specific; however, the fungal genera Fusarium , Filobasidium , Tilletiopsis , Alternaria , and Aureobasidium were indicator taxa shared among species. Overall, the larvae harbored 29% of unique taxa that can play a functional role in the host (e.g., initiation of gall development or selection of the mycelia composition). The mycobiome of the gall interior was assembled least stochastically, and its composition was the least species-specific, being dominated by Botryosphaeria dothidea (except for Lasioptera arundinis ). Therefore, the interior of ambrosia galls offers a unique environment that supports the growth of similar fungi, regardless of the host plant species and the phylogenetic distance between the AGM tribes. Our study illustrates a range of fungal microorganisms indicative of individual gall compartments, but their potential function, especially in larvae, remains to be solved. IMPORTANCE Ambrosia gall midges are endophagous insect herbivores whose larvae live enclosed within a single gall for their entire development period. They may exhibit phytomycetophagy, a remarkable feeding mode that involves the consumption of plant biomass and mycelia of their cultivated gall symbionts. Thus, AGMs are ideal model organisms for studying the role of microorganisms in the evolution of host specificity in insects. However, compared to other fungus-farming insects, insect–fungus mutualism in AGMs has been neglected. Our study is the first to use DNA metabarcoding to characterize the complete mycobiome of the entire system of the gall-forming insects as we profiled gall surfaces, nutritive mycelia, and larvae. Interestingly, larval mycobiomes were significantly different from their nutritive mycelia, although Botryosphaeria dothidea dominated the nutritive mycelia, regardless of the evolutionary separation of the tribes studied. Therefore, we confirmed a long-time hypothesized paradigm for the important evolutionary association of this fungus with AGMs.

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Seasonal Shifts in Bacterial and Fungal Microbiomes of Leaves and Associated Leaf-Mining Larvae Reveal Persistence of Core Taxa Regardless of Diet

Cited by 13 publications

References 118 publications

Seasonal dynamics of phyllosphere epiphytic microbial communities of medicinal plants in farmland environment

Seasonal dynamics of phyllosphere epiphytic microbial communities of medicinal plants in farmland environment

Middle Jurassic insect mines on gymnosperms provide missing links to early mining evolution

Mycobiomes of two distinct clades of ambrosia gall midges (Diptera: Cecidomyiidae) are species-specific in larvae but similar in nutritive mycelia

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