237 research outputs found

    Evolutionary ecology of obligate fungal and microsporidian invertebrate pathogens

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    The interactions between hosts and their parasites and pathogens are omnipresent in the natural world. These symbioses are not only key players in ecosystem functioning, but also drive genetic diversity through co-evolutionary adaptations. Within the speciose invertebrates, a plethora of interactions with obligate fungal and microsporidian pathogens exist, however the known interactions is likely only a fraction of the true diversity. Obligate invertebrate fungal and microsporidian pathogen require a host to continue their life cycle, some of which have specialised in certain host species and require host death to transmit to new hosts. Due to their requirement to kill a host to spread to a new one, obligate fungal and microsporidian pathogens regulate invertebrate host populations. Pathogen specialisation to a single or very few hosts has led to some fungi evolving the ability to manipulate their host’s behaviour to maximise transmission. The entomopathogenic fungus, Entomophthora muscae, infects houseflies (Musca domestica) over a week-long proliferation cycle, resulting in flies climbing to elevated positions, gluing their mouthparts to the substrate surface, and raising their wings to allow for a clear exit from fungal conidia through the host abdomen. These sequential behaviours are all timed to occur within a few hours of sunset. The E. muscae mechanisms used in controlling the mind of the fly remain relatively unknown, and whether other fitness costs ensue from an infection are understudied.European Commissio

    Microsporidian Infection in Mosquitoes (Culicidae) Is Associated with Gut Microbiome Composition and Predicted Gut Microbiome Functional Content

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    The animal gut microbiota consist of many different microorganisms, mainly bacteria, but archaea, fungi, protozoans, and viruses may also be present. This complex and dynamic community of microorganisms may change during parasitic infection. In the present study, we investigated the effect of the presence of microsporidians on the composition of the mosquito gut microbiota and linked some microbiome taxa and functionalities to infections caused by these parasites. We characterised bacterial communities of 188 mosquito females, of which 108 were positive for microsporidian DNA. To assess how bacterial communities change during microsporidian infection, microbiome structures were identified using 16S rRNA microbial profiling. In total, we identified 46 families and four higher taxa, of which Comamonadaceae, Enterobacteriaceae, Flavobacteriaceae and Pseudomonadaceae were the most abundant mosquito-associated bacterial families. Our data suggest that the mosquito gut microbial composition varies among host species. In addition, we found a correlation between the microbiome composition and the presence of microsporidians. The prediction of metagenome functional content from the 16S rRNA gene sequencing suggests that microsporidian infection is characterised by some bacterial species capable of specific metabolic functions, especially the biosynthesis of ansamycins and vancomycin antibiotics and the pentose phosphate pathway. Moreover, we detected a positive correlation between the presence of microsporidian DNA and bacteria belonging to Spiroplasmataceae and Leuconostocaceae, each represented by a single species, Spiroplasma sp. PL03 and Weissella cf. viridescens, respectively. Additionally, W. cf. viridescens was observed only in microsporidian-infected mosquitoes. More extensive research, including intensive and varied host sampling, as well as determination of metabolic activities based on quantitative methods, should be carried out to confirm our results.Peer reviewe

    Living in an infectious world: host‚Äďpathogen interactions shape social immunity in termites

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    Eusocial insect colonies can function like a single organism, a trait sometimes referred to as ‚Äúsuperorganism‚ÄĚ. Although superorganisms greatly benefit from division of labor, they may be susceptible to infectious diseases due to increased opportunities for pathogen transmission. The mechanisms behind insect societies‚Äô ability to successfully defend against infectious diseases are of significant interest in evolutionary biology. Next to their innate immune systems, eusocial insects such as termites boast sophisticated collective defences, termed social immunity, which are thought to have evolved in response to selective pressure from pathogens. Social immunity comprises a multi-layer assembly of physiological and behavioural adaptations which effectively supress the probability of exposure and transmission of infectious diseases within a colony. Although a significant body of research has explored the broad repertoire and effectiveness of termite collective defences, the underlying mechanisms of termite social immunity remain largely unexplored. This thesis exploits termite-pathogen step-wise infection dynamics to investigate the underlying mechanisms of collective defence against different entomopathogenic agents, as well as explore the link between innate defences and collective behaviours to offset increased disease pressure. The thesis is primarily based on research conducted in the eastern subterranean termite Reticulitermes flavipes and the entomopathogenic fungus Metarhizium anisopliae; a natural host‚Äďpathogen system. In Chapter I, we seek to explore the underpinnings of the ‚Äúcare-kill dichotomy‚ÄĚ in termite social immunity. The care-kill switch represents a generalized social immune response found in many advanced insect societies, whereby compromised nestmates are cared for when possible but sacrificed if necessary. In the case of fungal infection, we ask whether termites can detect and respond to infected individuals when pathogens (or infectious conidia) are absent from their cuticle; the rationale being to experimentally manipulate the type of cues that are presented to interacting nestmates. In this chapter, we sought to identify potential triggers for the switch from sanitary care to elimination defence (cannibalism), which represents the so-called care-kill transition. We sought to demonstrate how R. flavipes termites detect and respond to internal M. anisopliae infection at different stages of infection progression, as well as test the effect of pathogen viability on social immunity. By injecting fungal blastospores directly into the hemocoel of individuals, we removed the pathogen as a direct cue that could be detected by responding nestmates. Injection, regardless of blastospore viability, led to slightly increased rates of grooming, but also rapid transition to cannibalism (even at early stages of an internal infection), particularly when termites became visibly moribund following injection with viable blastospores. Surprisingly, however, cannibalism was still observed when termites were injected with dead blastospores and were not terminally ill, indicating that the threshold at which elimination behaviour is triggered can be reached at a very early stage during internal M. anisopliae infection, before viability or even terminal disease status is known. The faster cannibalism response to viable blastospore-injected termites could be due to the active synthesis of virulence factors from the pathogen such as destruxins, although this remains to be tested. Since termites may be expected to communicate with their nestmates via chemical compounds called cuticular hydrocarbons (CHCs), alterations in the CHCs profile associated with internal fungal pathogen presence, could represent important signals for responding nestmates. We used gas chromatography mass spectrometry (GC‚ÄďMS) in the second part of Chapter I to identify cues associated with disease status and explore potential CHC signal(s) that may be responsible for triggering elimination behaviours. We found that CHC profiles were significantly altered in individuals injected with viable but not dead blastospores, and at 15 but not at 12 hours post infection. More specifically, we detected significant increases in four exclusively methyl-branched CHCs 15 hours after injection with viable blastospores compared to control-injected individuals, which we speculate could be correlated with the advanced state of moribundity of these challenged individuals, and which may contribute as possible chemical cues triggering the high levels of observed cannibalism. Although a direct link between the identified CHC compounds and altered social immune behaviour remain to be tested, these data suggest that termites could employ chemical signals provoked by early internal immune activation to trigger cannibalism. In Chapter II we expand on the role of social immunity against potentially novel infection threats, as well as further explore the conditions that trigger specific behavioural defences. To understand the interaction between R. flavipes and the non-native entomopathogenic bacterium Pseudomonas entomophila and compare termites‚Äô collective defences between a native fungal entomopathogen and a non-native bacterium as well as characterize associated cuticular hydrocarbon (CHC) changes. We injected termites with different doses of either viable / dead P. entomophila or viable / dead M. anisopliae blastospores. As expected, injection regardless of severity and pathogen type led to slightly increased rates of grooming but rapid transition to cannibalism. Cannibalism was particularly evident when infected individuals were injected with high doses of viable P. entomophila and M. anisopliae blastospores (causing 100% mortality). Such individuals showed external signs of disease and were close to death, but as described in Chapter I, cannibalism was still exhibited following injection with dead blastospores, which elicited only 40% mortality. Interestingly, injection with an equivalent dose of viable P. entomophila (causing 40% mortality) did not elicit similarly elevated amounts of cannibalism, suggesting that triggers stimulating elimination behaviours may be pathogen-specific in this termite. We hypothesize that termites may have evolved greater sensitivity to fungal versus non-native bacterial infection, due to the likely long evolutionary association with the former. These results nevertheless show that collective defences of R. flavipes are effective against both fungal and bacterial challenges, with elimination behaviours being transferable to diverse and potentially novel infection threats (like P. entomophila). Analysis of CHC profiles from termites injected with different bacterial and fungal doses revealed unique patterns of CHCs, with a discriminant analysis showing a particularly distinct profile in termites injected with viable blastospores ‚ąí treatment associated with the strongest cannibalism response. In Chapter III, we examined the inhibition effect of the external antifungal activity of the Gram-negative binding protein 2 (GNBP-2) and collective behaviours after exposure of single individuals to M. anisopliae. Termites may depend on the innate immune system for defence against pathogens. Therefore, immune effectors have been co-opted from an internal role to an external role to prevent infection from entomopathogenic fungi that can evade innate immune defences after penetration of the cuticle. Termicins and GNBP-2 associated ő≤-1,3- glucanase activity are involved in external defence against M. anisopliae. The effectiveness of this external defence strategy likely depends on or is bolstered by collective behaviours. Through the suppression by an inhibitor (D-d-gluconolactone (GDL)) of the termite GNBP-2 ő≤- 1,3-glucanase activity that is capable of degrading entomopathogenic fungi, we found that collective defences such as grooming are not triggered, but instead cannibalistic behaviours are reduced. This suggests that the internal immune system or the use of antimicrobial secretions may be linked to certain collective immune behaviours in termites. Understanding the molecular basis of termite defence mechanisms may also be relevant for the development of sustainable control strategies against pest termite species. Finally, on the side of the pathogen, we require efficient transformation methods for entomopathogenic fungi to develop essential molecular tools for elucidating the function of genes involved in fungus-insect interactions. For example, by inserting or deleting genetic elements in the genome of the strain of interest, it is possible to modify the expression of targeted endogenous genes, and thereby experimentally test their role in the pathogen‚Äôs infection strategy, and how they may influence host fitness, immunity, and ultimately, social immune traits. However, developing methods to deliver foreign nucleic acid into fungal cells represents a major stumbling block in fungal genetics. In Chapter IV we address this issue by testing suitable selection markers: glufosinate ammonium (GFS) and chlorimuron ethyl (CME) for transformation of M. anisopliae with green fluorescence protein gene (gfp). Since M. anisopliae can produce blastospores through yeast-like budding in liquid culture, as well as being thin-walled and unicellular, an efficient blastospore-based transformation system was developed for the introduction of ‚Äúbar-gfp‚ÄĚ and ‚Äúsur-gfp‚ÄĚ constructs using the LiAc/ssDNA/PEG method. These genetic constructs conferred resistance to GFS and CME, respectively. We efficiently achieved integration of these genes into the fungal genome, resulting in resistant transformants, MA-0001 (baR-gfp) and MA-0002 (suR-gfp), which expressed high levels of green fluorescence in conidia, hyphae, blastospores, as well as on termite cadavers after injection of blastospores within the host hemolymph. The generation of these stable MA-0001 and MA-0002 strains allows us to monitor the internal infection process that begins after the fungus penetrates the cuticle and proliferates inside the termite hemolymph as hyphal bodies. This research represents a proof-of-principle that the genetic manipulation of M. anisopliae for studying gene function and for elucidating the relevant factors for pathogenic interactions with insects, is feasible. Targets for future work could include the generation of strains lacking virulence factors such as destruxins and examining the individual and social immune consequences of infection with genetically modified fungi. The present work highlights the importance of the effective innate immune responses in addition to physiological and behavioural defences in the termite R. flavipes, and how these are mediated by precise chemical communication which also contribute to social immunity. This allows R. flavipes to be less susceptible to pathogen infections and facilitates its evolutionary success

    Evaluating wild and commercial populations of Bombus terrestris ssp. audax (Harris, 1780): from genotype to phenotype.

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    Bees, including bumblebees, are highly valued for the pollination services they provide to natural ecosystems and agricultural crops. However, many bee species are facing declines, likely a result of habitat loss, pesticide use and climate change. Additionally, the use of imported commercial bumblebee colonies for crop pollination poses several risks to wild pollinators, including competition, hybridisation and pathogen spillover. A stock-take is needed of wild bees on both genetic and functional levels to identify vulnerable populations, detect local adaptations and to prevent further pollinator losses. We examine wild Irish B. terrestris ssp. audax on genomic, proteomic, and behavioural levels with reference to British and commercial populations to deepen our understanding of the selective processes acting on wild and domesticated bumblebee populations. We find that wild Irish and British populations of B. t. audax are distinctive on genomic levels and exhibit differential signatures of selection. We also find putative evidence for genetic distinctions between wild and commercial populations. A genomic examination of canonical immune genes in wild, Irish bumblebees highlighted several genes undergoing positive, purifying and possibly balancing selection, possibly reflecting their functional diversity and indicating recent adaptation. We uncover distinctions in the proteomes of wild and commercial lineages of lab-reared worker bee fat bodies and brains, as well as in the proteomic responses of these organs to pesticide exposure and infection. Finally, distinctions in the growth dynamics of wild and commercial lineages of B. t. audax colonies were identified alongside differences in the bacterial and fungal gut microbiomes of lab-reared wild and commercial workers. Overall, the findings of this thesis provide novel insights into the genetic, physiological, and behavioural distinctions between wild and domesticated populations of B. t. audax which will likely have major implications for how we conserve valuable genetic resources and manage commercial bumblebee imports

    The complex interactions between nutrition, immunity and infection in insects

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    Insects are the most diverse animal group on the planet. Their success is reflected by the diversity of habitats in which they live. However, these habitats have undergone great changes in recent decades; understanding how these changes affect insect health and fitness is an important challenge for insect conservation. In this Review, we focus on the research that links the nutritional environment with infection and immune status in insects. We first discuss the research from the field of nutritional immunology, and we then investigate how factors such as intracellular and extracellular symbionts, sociality and transgenerational effects may interact with the connection between nutrition and immunity. We show that the interactions between nutrition and resistance can be highly specific to insect species and/or infection type ‚Äď this is almost certainly due to the diversity of insect social interactions and life cycles, and the varied environments in which insects live. Hence, these connections cannot be easily generalised across insects. We finally suggest that other environmental aspects ‚Äď such as the use of agrochemicals and climatic factors ‚Äď might also influence the interaction between nutrition and resistance, and highlight how research on these is essential

    Investigating the effects of glyphosate on the bumblebee proteome and microbiota

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    Glyphosate is one of the most widely used herbicides globally. It acts by inhibiting an enzyme in an aromatic amino acid synthesis pathway specific to plants and microbes, leading to the view that it poses no risk to other organisms. However, there is growing concern that glyphosate is associated with health effects in humans and an ever-increasing body of evidence that suggests potential deleterious effects on other animals including pollinating insects such as bees. Although pesticides have long been considered a factor in the decline of wild bee populations, most research on bees has focussed on demonstrating and understanding the effects of insecticides. To assess whether glyphosate poses a risk to bees, we characterised changes in survival, behaviour, sucrose solution consumption, the digestive tract proteome, and the microbiota in the bumblebee Bombus terrestris after chronic exposure to field relevant doses of technical grade glyphosate or the glyphosate-based formulation, RoundUp Optima+¬ģ. Regardless of source, there were changes in response to glyphosate exposure in important cellular and physiological processes in the digestive tract of B. terrestris, with proteins associated with oxidative stress regulation, metabolism, cellular adhesion, the extracellular matrix, and various signalling pathways altered. Interestingly, proteins associated with endocytosis, oxidative phosphorylation, the TCA cycle, and carbohydrate, lipid, and amino acid metabolism were differentially altered depending on whether the exposure source was glyphosate alone or RoundUp Optima+¬ģ. In addition, there were alterations to the digestive tract microbiota of bees depending on the glyphosate source No impacts on survival, behaviour, or food consumption were observed. Our research provides insights into the potential mode of action and consequences of glyphosate exposure at the molecular, cellular and organismal level in bumblebees and highlights issues with the current honeybee-centric risk assessment of pesticides and their formulations, where the impact of co-formulants on non-target organisms are generally overlooked

    Assessment of the ecotoxicological health status of Apis mellifera using a multi-tier approach based on biomarkers, proteomic analysis and quality and origin of bee products

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    Pollinating insects play a role of primary importance both in agriculture, ensuring the crops productivity, and in the conservation of plant biodiversity. Among pollinators, Apis mellifera L., 1958 (Hymenoptera: Apidae) is the most known and widespread species and the most valuable for its pollination service. This species is disappearing globally due to different reasons, such as climate change, the massive use of Plant Protection Products (PPPs) and other environmental contaminants diffusion, habitat fragmentation and parasites infections. The sub-lethal levels of pesticide residues and other anthropic contaminants, even not leading to the death of individuals, are able to cause problems in the development, behaviour and health of animals in the short and long term. Moreover, honey bees are exposed to mixtures of contaminants in the environment, that can cause different effects. However, there is a large gap in the assessment of the sub-lethal effects of these mixtures. Another gap in the research on the ecotoxicology of these animals is the assessment of the effects of commercial formulates instead of only using the active principles. Among the sub-lethal effects that were examined in the literature relating to pesticides exposure, rarely genotoxicity and immune system biomarkers were used. Anthropic activities could also be able to modify indirectly the quality and origin of bee products, since they can alter honey bees health and consequently their productivity. The use of an integrated approach to combine responses at different levels, could be a valid tool to evaluate the impact of contamination on these organisms. The goal of this thesis was to assess the health of honey bee colonies using a multi-tier methodology that included biomarker responses, proteomic analysis, and bee product quality and origin. This thesis was divided in two parts: ‚óŹ A laboratory study, exposing Apis mellifera specimens to two commercial pesticides, the fungicide Sakura¬ģ and the herbicide Elegant 2FD, alone and in combination. The effects of these compounds were assessed integrating two methodologies, consisting in a set of biomarkers and a proteomics approach. Both pesticides modulated the detoxification process. The fungicide alone had also effects on the metabolism, while the herbicide demonstrated to be neurotoxic. The results from the mixture treatments demonstrated that the effects obtained were influenced mostly by the herbicide. The proteomic approach revealed that the two pesticides were able to affect the energy metabolism, the immune system and the protein synthesis. The proteomic approach should be improved to understand if and to what extent the above-mentioned post-translational changes happened, using specific antibodies to perform a more specific assessment. ‚óŹ A two-year monitoring study, aiming to assess the ecotoxicological status of bees in natural environments. Apis mellifera specimens were sampled in 10 locations in Tuscany region characterised by varying contamination patterns. In this case, the used approach was made up of a set of biomarkers, used to assess the health status of honey bees, and the analyses of origin and quality of the honey, through melissopalynological and chemical-physical analyses. The biomarkers results obtained for the first year showed that the suburban area and the agricultural area were undergoing major stress but with different kinds of effects, probably because the contaminants were different in the various areas. In 2021 the specimens undergoing major stress were the ones coming from vineyards, that showed genotoxic effects, and clover field and wheat crops, showing alterations in nervous and immune systems. The comparison between the 2 years results showed that the organisms were undergoing major stress condition in 2021 compared to 2020. Bees from 2021 reported neurotoxic effects, the presence of oxidative stress and DNA damage. The different responses obtained could be due not only to contaminants but also to the changing of climatic conditions, such as differences in temperatures and rainfalls, which were also taken into consideration. The melissopalynological analysis showed that only in the clover field the pollen derived from the cultivation that we observed during the sampling. These findings suggest that the biomarker responses observed in A. mellifera specimens are probably not due to pollen contamination. In fact, organisms could come in contact with contaminants through other exposure routes. The carbohydrates, amino acids and humidity analysis showed that honey samples were not characterised by major differences, even if coming from different areas, except for the proportion of some amino acids, due to the presence of different pollens. Both the studies had also the goal to start filling a research gap regarding the assessment of effects on immune system and DNA damages, obtaining promising results. The integrated approaches that were used proved to be effective to observe the ecotoxicological health status of Apis mellifera from different points of view. The multi-trial approach would be a sensitive tool to measure sub-lethal effects, and not only lethal ones, of pesticide active principles and, more important, of pesticide commercial formulations. It would be helpful to improve the current risk assessment procedure for chemical registration and use, making the agricultural environment more pollinator-friendly

    New insights into the genome and transmission of the microsporidian pathogen Nosema muscidifuracis

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    IntroductionNosema is a diverse genus of unicellular microsporidian parasites of insects and other arthropods. Nosema muscidifuracis infects parasitoid wasp species of Muscidifurax zaraptor and M. raptor (Hymenoptera: Pteromalidae), causing ~50% reduction in longevity and‚ÄČ~90% reduction in fecundity.Methods and ResultsHere, we report the first assembly of the N. muscidifuracis genome (14,397,169‚ÄČbp in 28 contigs) of high continuity (contig N50 544.3 Kb) and completeness (BUSCO score 97.0%). A total of 2,782 protein-coding genes were annotated, with 66.2% of the genes having two copies and 24.0% of genes having three copies. These duplicated genes are highly similar, with a sequence identity of 99.3%. The complex pattern suggests extensive gene duplications and rearrangements across the genome. We annotated 57 rDNA loci, which are highly GC-rich (37%) in a GC-poor genome (25% genome average). Nosema-specific qPCR primer sets were designed based on 18S rDNA annotation as a diagnostic tool to determine its titer in host samples. We discovered high Nosema titers in Nosema-cured M. raptor and M. zaraptor using heat treatment in 2017 and 2019, suggesting that the remedy did not completely eliminate the Nosema infection. Cytogenetic analyses revealed heavy infections of N. muscidifuracis within the ovaries of M. raptor and M. zaraptor, consistent with the titer determined by qPCR and suggesting a heritable component of infection and per ovum vertical transmission.DiscussionThe parasitoids-Nosema system is laboratory tractable and, therefore, can serve as a model to inform future genome manipulations of Nosema-host system for investigations of Nosemosis

    Investigating the effects of non-insecticide pesticides widely used in Irish agriculture on the bumblebee Bombus terrestris (L. 1758)

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    Although pesticides are a key driver of bee decline globally, the contribution of non-insecticidal pesticides, specifically herbicides and fungicides, is poorly understood. The herbicide glyphosate and the fungicide prothioconazole are amongst the most widely used pesticides in Ireland. Consequently, characterising their impact on Ireland‚Äôs wild bee species is of urgent importance. Here, I investigated and characterised the impact of glyphosate and prothioconazole on the bumblebee B. terrestris at the molecular and organism level, in addition to two representative commercial formulations: Roundup Optima+¬ģ and Proline¬ģ, containing glyphosate and prothioconazole, respectively. Utilising mass spectrometry-based proteomics, DNA amplicon sequencing, and survival assays, I uncovered the impact of these pesticides and formulations on the digestive tract, brain, and fat body proteome, digestive tract microbiota, survival, behaviour, and food consumption in B. terrestris. Neither pesticide altered survival or food consumption, but prothioconazole altered behaviour at field-realistic concentrations. Further, all treatments led to microbiota dysbiosis. Glyphosate and Roundup Optima+¬ģ consistently altered oxidative stress regulation and mitochondrial proteins in all organs and led to decreases in structural proteins in the digestive tract. Both glyphosate-based treatments altered synaptic transmission and signaling in the brain, and protein biosynthesis and energy homeostasis in the fat body. However, differential impacts were also observed. Further, prothioconazole and Proline¬ģ had differential impacts on all key organs, indicating the impact of co-formulants in formulations and solvents used for pesticide solubility on bees, leading to significant alterations to detoxification, neurotransmitter biosynthesis and cytoskeletal proteins, and oxidative stress in the digestive tract, brain, and fat body, respectively. Overall, this research uncovered the impacts of glyphosate and prothioconazole, as well as representative formulations, on B. terrestris, and raised important questions on the complexities of pesticide impacts on bees when used as part of a formulation

    Environment or genetic isolation? An atypical intestinal microbiota in the Maltese honeybee Apis mellifera spp. ruttneri

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    Apis mellifera evolved mainly in African, Asian and European continents over thousands of years, leading to the selection of a considerable number of honey bees subspecies that have adapted to various environments such as hot semi-desert zones and cold temperate zones. With the evolution of honey bee subspecies, it is possible that environmental conditions, food sources and microbial communities typical of the colonised areas have shaped the honey bee gut microbiota. In this study the microbiota of two distinct lineages (mitochondrial haplotypes) of bees Apis mellifera ruttneri (lineage A) and Apis mellifera ligustica and carnica (both lineage C) were compared. Honey bee guts were collected in a dry period in the respective breeding areas (the island of Malta and the regions of Emilia-Romagna and South Tyrol in Italy). Microbial DNA from the honey bee gut was extracted and amplified for the V3-V4 regions of the 16S rRNA gene for bacteria and for ITS2 for fungi. The analyses carried out show that the Maltese lineage A honey bees have a distinctive microbiota when compared to Italian lineage C honey bees, with the most abundant genera being Bartonellaceae and Lactobacillaceae, respectively. Lactobacillaceae in Maltese Lineage A honey bees consist mainly of Apilactobacillus instead of Lactobacillus and Bombilactobacillus in the lineage C. Lineage A honey bee gut microbiota also harbours higher proportions of Arsenophonus, Bombella, Commensalibacter and Pseudomonas when compared to lineage C. The environment seems to be the main driver in the acquisition of these marked differences in the gut microbiota . However, the influence of other factors such as host genetics, seasonality or geography may still play a significant role in the microbiome shaping, in synergy with the environmental aspects
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