Some pathogenic phloem‐limited bacteria are a major threat for worldwide agriculture due to the heavy economic losses caused to many high‐value crops. These disease agents – phytoplasmas, ...spiroplasmas, liberibacters, and Arsenophonus‐like bacteria – are transmitted from plant to plant by phloem‐feeding Hemiptera vectors. The associations established among pathogens and vectors result in a complex network of interactions involving also the whole microbial community harboured by the insect host. Interactions among bacteria may be beneficial, competitive, or detrimental for the involved microorganisms, and can dramatically affect the insect vector competence and consequently the spread of diseases. Interference is observed among pathogen strains competing to invade the same vector specimen, causing selective acquisition or transmission. Insect bacterial endosymbionts are another pivotal element of interactions between vectors and phytopathogens, because of their central role in insect life cycles. Some symbionts, either obligate or facultative, were shown to have antagonistic effects on the colonization by plant pathogens, by producing antimicrobial substances, by stimulating the production of antimicrobial substances by insects, or by competing for host infection. In other cases, the mutual exclusion between symbiont and pathogen suggests a possible detrimental influence on phytopathogens displayed by symbiotic bacteria; conversely, examples of microbes enhancing pathogen load are available as well. Whether and how bacterial exchanges occurring in vectors affect the relationship between insects, plants, and phytopathogens is still unresolved, leaving room for many open questions concerning the significance of particular traits of these multitrophic interactions. Such complex interplays may have a serious impact on pathogen spread and control, potentially driving new strategies for the containment of important diseases.
Phloem‐limited bacterial phytopathogens, transmitted among plants by phloem‐feeding Hemiptera vectors, cause heavy losses in agriculture. Associations of pathogens and vectors form complex networks of interactions involving also the microbial community harboured by the insect host; bacterial interactions may have beneficial or detrimental influences on a vector's efficacy. How such complex interplays affect insect‐plant‐bacteria interactions is still unresolved; however, their impact on pathogen spread and control could drive new strategies for the containment of important diseases.
Summary
Popillia japonica Newman (Coleoptera: Scarabaeidae) is a highly polyphagous invasive beetle originating from Japan. This insect is highly resilient and able to rapidly adapt to new ...vegetation. Insect‐associated microorganisms can play important roles in insect physiology, helping their hosts to adapt to changing conditions and potentially contributing to an insect's invasive potential. Such symbiotic bacteria can be part of a core microbiota that is stably transmitted throughout the host's life cycle or selectively recruited from the environment at each developmental stage. The aim of this study was to investigate the origin, stability and turnover of the bacterial communities associated with an invasive population of P. japonica from Italy. Our results demonstrate that soil microbes represent an important source of gut bacteria for P. japonica larvae, but as the insect develops, its gut microbiota richness and diversity decreased substantially, paralleled by changes in community composition. Notably, only 16.75% of the soil bacteria present in larvae are maintained until the adult stage. We further identified the micro‐environments of different gut sections as an important factor shaping microbiota composition in this species, likely due to differences in pH, oxygen availability and redox potential. In addition, P. japonica also harboured a stable bacterial community across all developmental stages, consisting of taxa well known for the degradation of plant material, namely the families Ruminococcacae, Christensenellaceae and Lachnospiraceae. Interestingly, the family Christensenallaceae had so far been observed exclusively in humans. However, the Christensenellaceae operational taxonomic units found in P. japonica belong to different taxonomic clades within this family.
Intracellular reproductive manipulators, such as Candidatus Cardinium and Wolbachia are vertically transmitted to progeny but rarely show co-speciation with the host. In sap-feeding insects, plant ...tissues have been proposed as alternative horizontal routes of interspecific transmission, but experimental evidence is limited. Here we report results from experiments that show that Cardinium is horizontally transmitted between different phloem sap-feeding insect species through plants. Quantitative PCR and in situ hybridization experiments indicated that the leafhopper Scaphoideus titanus releases Cardinium from its salivary glands during feeding on both artificial media and grapevine leaves. Successional time-course feeding experiments with S. titanus initially fed sugar solutions or small areas of grapevine leaves followed by feeding by the phytoplasma vector Macrosteles quadripunctulatus or the grapevine feeder Empoasca vitis revealed that the symbionts were transmitted to both species. Explaining interspecific horizontal transmission through plants improves our understanding of how symbionts spread, their lifestyle and the symbiont-host intermixed evolutionary pattern.
The family Pentatomidae (Hemiptera: Heteroptera) includes several invasive stink bug species capable to attack a large number of wild and cultivated plants, causing several damages to different ...crops. Pentatomids rely on obligate symbiotic associations with bacteria of the family
, mainly of the genus
. A distinctive trait of these associations is the transmission route: during oviposition, females smear egg masses with symbiont-containing secretions, which are ingested by newly hatched nymphs, allowing the symbiont to pass through their digestive tract and establish in the crypts of the posterior midgut. Preventing newborns from orally acquiring symbionts seriously affects their fitness and survival. This symbiont inheritance process can be manipulated to develop innovative pest control measures by sterilization of egg masses prior to nymph hatching. This review summarizes the recent knowledge advances concerning the gut primary symbionts of pentatomids, with a specific focus on the most troubling pest species for agriculture. Current understanding of host colonization dynamics in pentatomids is presented, as well as the phenotypic effects determined in different insect species by the alteration of vertical transmission. Details on the current knowledge on the whole bacterial communities accompanying primary symbionts are analyzed. The recent research exploiting the perturbation of symbiont acquisition by pentatomid nymphs is discussed, by considering published work on laboratory and field trials with several active substances. These translational strategies are presently regarded as promising for limiting the populations of many important pentatomid pests in a sustainable way.
Insect immunity is a crucial process in interactions between host and microorganisms and the presence of pathogenic, commensal, or beneficial bacteria may result in different immune responses. In ...Hemiptera vectors of phytoplasmas, infected insects are amenable to carrying high loads of phytopathogens, besides hosting other bacterial affiliates, which have evolved different strategies to be retained; adaptation to host response and immunomodulation are key aspects of insect-symbiont interactions. Most of the analyses published to date has investigated insect immune response to pathogens, whereas few studies have focused on the role of host immunity in microbiota homeostasis and vectorial capacity. Here the expression of immune genes in the leafhopper vector of phytoplasmas
was investigated following exposure to
symbiotic bacteria, previously demonstrated to affect phytoplasma acquisition by leafhoppers. The expression of four genes related to major components of immunity was measured, i.e., defensin, phenoloxidase, kazal type 1 serine protease inhibitor and Raf, a component of the Ras/Raf pathway. The response was separately tested in whole insects, midguts and cultured hemocytes. Healthy individuals were assessed along with specimens undergoing early- and late-stage phytoplasma infection. In addition, the adhesion grade of
strains was examined to assess whether symbionts could establish a physical barrier against phytoplasma colonization. Our results revealed a specific activation of Raf in midguts after double infection by
and flavescence dorée phytoplasma. Increased expression was observed already in early stages of phytoplasma colonization. Gut-specific localization and timing of Raf activation are consistent with the role played by
in limiting phytoplasma acquisition by
, supporting the involvement of this gene in the anti-pathogen activity. However, limited attachment capability was found for
under
experimental conditions, suggesting a minor contribution of physical phytoplasma exclusion from the vector gut wall. By providing evidence of immune modulation played by
, these results contribute to elucidating the molecular mechanisms regulating interference with phytoplasma infection in
. The involvement of Raf suggests that in the presence of reduced immunity (reported in Hemipterans), immune genes can be differently regulated and recruited to play additional functions, generally played by genes lost by hemipterans.
The core gut microbiome of adult honeybee comprises a set of recurring bacterial phylotypes, accompanied by lineage-specific, variable, and less abundant environmental bacterial phylotypes. Several ...mutual interactions and functional services to the host, including the support provided for growth, hormonal signaling, and behavior, are attributed to the core and lineage-specific taxa. By contrast, the diversity and distribution of the minor environmental phylotypes and fungal members in the gut remain overlooked. In the present study, we hypothesized that the microbial components of forager honeybees (i.e., core bacteria, minor environmental phylotypes, and fungal members) are compartmentalized along the gut portions. The diversity and distribution of such three microbial components were investigated in the context of the physico-chemical conditions of different gut compartments. We observed that changes in the distribution and abundance of microbial components in the gut are consistently compartment-specific for all the three microbial components, indicating that the ecological and physiological interactions among the host and microbiome vary with changing physico-chemical and metabolic conditions of the gut.
Bacteria of the genus Asaia have been recently recognized as secondary symbionts of different sugar-feeding insects, including the leafhopper Scaphoideus titanus, vector of Flavescence dorée ...phytoplasmas. Asaia has been shown to be localized in S. titanus gut, salivary glands and gonoducts and to be maternally transmitted to the progeny by an egg smearing mechanism. It is currently not known whether Asaia in S. titanus is transmitted by additional routes. We performed a study to evaluate if Asaia infection is capable of horizontal transmission via co-feeding and venereal routes.
A Gfp-tagged strain of Asaia was provided to S. titanus individuals to trace the transmission pathways of the symbiotic bacterium. Co-feeding trials showed a regular transfer of bacterial cells from donors to recipients, with a peak of frequency after 72 hours of exposure, and with concentrations of the administrated strain growing over time. Venereal transmission experiments were first carried out using infected males paired with uninfected females. In this case, female individuals acquired Gfp-labelled Asaia, with highest infection rates 72-96 hours after mating and with increasing abundance of the tagged symbiont over time. When crosses between infected females and uninfected males were conducted, the occurrence of "female to male" transmission was observed, even though the transfer occurred unevenly.
The data presented demonstrate that the acetic acid bacterial symbiont Asaia is horizontally transmitted among S. titanus individuals both by co-feeding and venereal transmission, providing one of the few direct demonstrations of such a symbiotic transfer in Hemiptera. This study contributes to the understanding of the bacterial ecology in the insect host, and indicates that Asaia evolved multiple pathways for the colonization of S. titanus body.
Summary
The pivotal role of diet in shaping gut microbiota has been evaluated in different animal models, including insects. Drosophila flies harbour an inconstant microbiota among which acetic acid ...bacteria (AAB) are important components. Here, we investigated the bacterial and AAB components of the invasive pest Drosophila suzukii microbiota, by studying the same insect population separately grown on fruit‐based or non‐fruit artificial diet. AAB were highly prevalent in the gut under both diets (90 and 92% infection rates with fruits and artificial diet respectively). Fluorescent in situ hybridization and recolonization experiments with green fluorescent protein (Gfp)‐labelled strains showed AAB capability to massively colonize insect gut. High‐throughput sequencing on 16S rRNA gene indicated that the bacterial microbiota of guts fed with the two diets clustered separately. By excluding AAB‐related OTUs from the analysis, insect bacterial communities did not cluster separately according to the diet, suggesting that diet‐based diversification of the community is primarily reflected on the AAB component of the community. Diet influenced also AAB alpha‐diversity, with separate OTU distributions based on diets. High prevalence, localization and massive recolonization, together with AAB clustering behaviour in relation to diet, suggest an AAB role in the D. suzukii gut response to diet modification.
Some species of acetic acid bacteria (AAB) play relevant roles in the metabolism and physiology of
Drosophila
spp. and in some cases convey benefits to their hosts. The pest
Drosophila suzukii
...harbors a set of AAB similar to those of other
Drosophila
species. Here, we investigate the potential to exploit the ability of AAB to produce volatile substances that attract female
D. suzukii
. Using a two-way olfactometer bioassay, we investigate the preference of
D. suzukii
for strains of AAB, and using solid-phase microextraction gas chromatography–mass spectrometry we specifically characterize their volatile profiles to identify attractive and non-attractive components produced by strains from the genera
Acetobacter
,
Gluconobacter,
and
Komagataeibacter
. Flies had a preference for one strain of
Komagataeibacter
and two strains of
Gluconobacter
. Analyses of the volatile profiles from the preferred
Gluconobacter
isolates found that acetic acid is distinctively emitted even after 2 days of bacterial growth, confirming the relevance of this volatile in the profile of this isolate for attracting flies. Analyses of the volatile profile from the preferred
Komagataeibacter
isolate showed that a different volatile in its profile could be responsible for attracting
D. suzukii
. Moreover, variation in the concentration of butyric acid derivatives found in some strains may influence the preference of
D. suzukii
. Our results indicate that
Gluconobacter
and
Komagataeibacter
strains isolated from
D. suzukii
have the potential to provide substances that could be exploited to develop sustainable mass-trapping-based control approaches.
Summary
Microorganisms establish with their animal hosts close interactions. They are involved in many aspects of the host life, physiology and evolution, including nutrition, reproduction, immune ...homeostasis, defence and speciation. Thus, the manipulation and the exploitation the microbiota could result in important practical applications for the development of strategies for the management of insect‐related problems. This approach, defined as ‘Microbial Resource Management’ (MRM), has been applied successfully in various environments and ecosystems, as wastewater treatments, prebiotics in humans, anaerobic digestion and so on. MRM foresees the proper management of the microbial resource present in a given ecosystem in order to solve practical problems through the use of microorganisms. In this review we present an interesting field for application for MRM concept, i.e. the microbial communities associated with arthropods and nematodes. Several examples related to this field of applications are presented. Insect microbiota can be manipulated: (i) to control insect pests for agriculture; (ii) to control pathogens transmitted by insects to humans, animals and plants; (iii) to protect beneficial insects from diseases and stresses. Besides, we prospect further studies aimed to verify, improve and apply MRM by using the insect–symbiont ecosystem as a model.
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