Insect-microbe interactions: the good, the bad and the others

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Unexpected diversity of Wolbachia associated with Bactrocera dorsalis (Diptera: Tephritidae) in Africa

Bactrocera dorsalis (Hendel) is an important pest of fruit-bearing plants in many countries worldwide. In Africa, this pest has spread rapidly and has become widely established since the first invasion report in 2003. Wolbachia is a vertically transmitted endosymbiont that can significantly influence aspects of the biology and, in particular, the reproduction of its host. In this study, we screened B. dorsalis specimens collected from several locations in Africa between 2005 and 2017 for Wolbachia using a PCR-based assay to target the Wolbachia surface protein wsp. Of the 357 individuals tested, 10 were positive for Wolbachia using the wsp assay. We identified four strains of Wolbachia infecting two B. dorsalis mitochondrial haplotypes. We found no strict association between the infecting strain and host haplotype, with one strain being present in two different host haplotypes. All the detected strains belonged to Super Group B Wolbachia and did not match any strains reported previously in B. dorsalis in Asia. These findings indicate that diverse Wolbachia infections are present in invasive populations of B. dorsalis

Mathematical modelling of the interactive dynamics of wild and Microsporidia MB-infected mosquitoes

AVAILABILITY OF DATA AND MATERIALS : All data generated or analysed during this study are included in this published article.The present study was executed by the International Centre of Insect Physiology and Ecology as part of the Symbiont Modeling and Deployment Strategies project, made possible by the generous support of the Bill and Melinda Gates Foundation.A recent discovery highlighted that mosquitoes infected with Microsporidia MB are unable to transmit the Plasmodium to humans. Microsporidia MB is a symbiont transmitted vertically and horizontally in the mosquito population, and these transmission routes are known to favor the persistence of the parasite in the mosquito population. Despite the dual transmission, data from field experiments reveal a low prevalence of MB-infected mosquitoes in nature. This study proposes a compartmental model to understand the prevalence of MB-infected mosquitoes. The dynamic of the model is obtained through the computation of the basic reproduction number and the analysis of the stability of the MB-free and coexistence equilibria. The model shows that, in spite of the high vertical transmission efficiency of Microsporidia MB, there can still be a low prevalence of MB-infected mosquitoes. Numerical analysis of the model shows that male-to-female horizontal transmission contributes more than female-to-male horizontal transmission to the spread of MB-infected mosquitoes. Moreover, the female-to-male horizontal transmission contributes to the spread of the symbiont only if there are multiple mating occurrences for male mosquitoes. Furthermore, when fixing the efficiencies of vertical transmission, the parameters having the greater influence on the ratio of MB-positive to wild mosquitoes are identified. In addition, by assuming a similar impact of the temperature on wild and MB-infected mosquitoes, our model shows the seasonal fluctuation of MB-infected mosquitoes. This study serves as a reference for further studies, on the release strategies of MB-infected mosquitoes, to avoid overestimating the MB-infection spread.http://www.aimspress.com/journal/mbeam2024Mathematics and Applied MathematicsSDG-03:Good heatlh and well-bein

Vertical transmission of a Drosophila endosymbiont via cooption of the yolk transport and internalization machinery

Spiroplasma is a diverse bacterial clade that includes many vertically transmitted insect endosymbionts, including Spiroplasma poulsonii, a natural endosymbiont of Drosophila melanogaster. These bacteria persist in the hemolymph of their adult host and exhibit efficient vertical transmission from mother to offspring. In this study, we analyzed the mechanism that underlies their vertical transmission, and here we provide strong evidence that these bacteria use the yolk uptake machinery to colonize the germ line. We show that Spiroplasma reaches the oocyte by passing through the intercellular space surrounding the ovarian follicle cells and is then endocytosed into oocytes within yolk granules during the vitellogenic stages of oogenesis. Mutations that disrupt yolk uptake by oocytes inhibit vertical Spiroplasma transmission and lead to an accumulation of these bacteria outside the oocyte. Impairment of yolk secretion by the fat body results in Spiroplasma not reaching the oocyte and a severe reduction of vertical transmission. We propose a model in which Spiroplasma first interacts with yolk in the hemolymph to gain access to the oocyte and then uses the yolk receptor, Yolkless, to be endocytosed into the oocyte. Cooption of the yolk uptake machinery is a powerful strategy for endosymbionts to target the germ line and achieve vertical transmission. This mechanism may apply to other endosymbionts and provides a possible explanation for endosymbiont host specificity. IMPORTANCE: Most insect species, including important disease vectors and crop pests, harbor vertically transmitted endosymbiotic bacteria. Studies have shown that many facultative endosymbionts, including Spiroplasma, confer protection against different classes of parasites on their hosts and therefore are attractive tools for the control of vector-borne diseases. The ability to be efficiently transmitted from females to their offspring is the key feature shaping associations between insects and their inherited endosymbionts, but to date, little is known about the mechanisms involved. In oviparous animals, yolk accumulates in developing eggs and serves to meet the nutritional demands of embryonic development. Here we show that Spiroplasma coopts the yolk transport and uptake machinery to colonize the germ line and ensure efficient vertical transmission. The uptake of yolk is a female germ line-specific feature and therefore an attractive target for cooption by endosymbionts that need to maintain high-fidelity maternal transmission

The fungus Leptosphaerulina persists in Anopheles gambiae and induces melanization

Anopheles mosquitoes are colonized by diverse microorganisms that may impact on host biology and vectorial capacity. Eukaryotic symbionts such as fungi have been isolated from Anopheles, but whether they are stably associated with mosquitoes and transmitted transstadially across mosquito life stages or to subsequent generations remains largely unexplored. Here, we show that a Leptosphaerulina sp. fungus isolated from the midgut of An. gambiae can be stably associated with An. gambiae host and that it imposes low fitness cost when re-introduced through co-feeding. This fungus is transstadially transmitted across An. gambiae developmental stages and to their progeny. It is present in field-caught larvae and adult mosquitoes at moderate levels across geographical regions. We observed that Leptosphaerulina sp. induces a distinctive melanotic phenotype across the developmental stages of mosquito. As a eukaryotic symbiont that is stably associated with An. gambiae Leptosphaerulina sp. can be explored for paratransgenesis

The Role of Lipid Competition for Endosymbiont-Mediated Protection against Parasitoid Wasps in Drosophila

Insects commonly harbor facultative bacterial endosymbionts, such as Wolbachia and Spiroplasma species, that are vertically transmitted from mothers to their offspring. These endosymbiontic bacteria increase their propagation by manipulating host reproduction or by protecting their hosts against natural enemies. While an increasing number of studies have reported endosymbiont-mediated protection, little is known about the mechanisms underlying this protection. Here, we analyze the mechanisms underlying protection from parasitoid wasps in Drosophila melanogaster mediated by its facultative endosymbiont Spiroplasma poulsonii. Our results indicate that S. poulsonii exerts protection against two distantly related wasp species, Leptopilina boulardi and Asobara tabida. S. poulsonii-mediated protection against parasitoid wasps takes place at the pupal stage and is not associated with an increased cellular immune response. In this work, we provide three important observations that support the notion that S. poulsonii bacteria and wasp larvae compete for host lipids and that this competition underlies symbiont-mediated protection. First, lipid quantification shows that both S. poulsonii and parasitoid wasps deplete D. melanogaster hemolymph lipids. Second, the depletion of hemolymphatic lipids using the Lpp RNA interference (Lpp RNAi) construct reduces wasp success in larvae that are not infected with S. poulsonii and blocks S. poulsonii growth. Third, we show that the growth of S. poulsonii bacteria is not affected by the presence of the wasps, indicating that when S. poulsonii is present, larval wasps will develop in a lipid-depleted environment. We propose that competition for host lipids may be relevant to endosymbiont-mediated protection in other systems and could explain the broad spectrum of protection provide

Mathematical modelling of the interactive dynamics of wild and <i>Microsporidia MB</i>-infected mosquitoes

A recent discovery highlighted that mosquitoes infected with Microsporidia MB are unable to transmit the Plasmodium to humans. Microsporidia MB is a symbiont transmitted vertically and horizontally in the mosquito population, and these transmission routes are known to favor the persistence of the parasite in the mosquito population. Despite the dual transmission, data from field experiments reveal a low prevalence of MB-infected mosquitoes in nature. This study proposes a compartmental model to understand the prevalence of MB-infected mosquitoes. The dynamic of the model is obtained through the computation of the basic reproduction number and the analysis of the stability of the MB-free and coexistence equilibria. The model shows that, in spite of the high vertical transmission efficiency of Microsporidia MB, there can still be a low prevalence of MB-infected mosquitoes. Numerical analysis of the model shows that male-to-female horizontal transmission contributes more than female-to-male horizontal transmission to the spread of MB-infected mosquitoes. Moreover, the female-to-male horizontal transmission contributes to the spread of the symbiont only if there are multiple mating occurrences for male mosquitoes. Furthermore, when fixing the efficiencies of vertical transmission, the parameters having the greater influence on the ratio of MB-positive to wild mosquitoes are identified. In addition, by assuming a similar impact of the temperature on wild and MB-infected mosquitoes, our model shows the seasonal fluctuation of MB-infected mosquitoes. This study serves as a reference for further studies, on the release strategies of MB-infected mosquitoes, to avoid overestimating the MB-infection spread

Differential immune responses in new and old fruit fly-parasitoid associations : implications for their management

The oriental fruit fly, Bactrocera dorsalis (Hendel), and marula fruit fly, Ceratitis cosyra (Walker), are major fruit-infesting tephritids across sub-Saharan Africa. Biological control of these pests using parasitic wasps has been widely adopted but with varying levels of success. Most studies investigating host-parasitoid models have focused on functional and evolutionary aspects leaving a knowledge gap about the physiological mechanisms underpinning the efficacy of parasitoids as biocontrol agents of tephritids. To better understand these physiological mechanisms, we investigated changes in the cellular immune responses of C. cosyra and B. dorsalis when exposed to the parasitic wasps, Diachasmimorpha longicaudata (Ashmaed) and Psyttalia cosyrae (Wilkinson). We found that B. dorsalis was more resistant to parasitisation, had a higher hemocyte count, and encapsulated more parasitoid eggs compared to C. cosyra, achieving up to 100% encapsulation when exposed to P. cosyrae. Exposing B. dorsalis to either parasitoid species induced the formation of a rare cell type, the giant multinucleated hemocyte, which was not observed in C. cosyra. Furthermore, compared to P. cosyrae-parasitized larvae, those of both host species parasitized by D. longicaudata had lower encapsulation rates, hemocyte counts and spreading abilities and yielded a higher number of parasitoid progeny with the highest parasitoid emergence (72.13%) recorded in C. cosyra. These results demonstrate that cellular immune responses are central to host-parasitoid interaction in tephritid fruit flies and further suggest that D. longicaudata presents greater potential as a biocontrol agent of B. dorsalis and C. cosyra in horticultural cropping systems.DATA AVAILABILITY STATEMENT: The datasets presented in this study can be found in online repositories. The names of the repository/repositories and accession number(s) can be found below: https://dmmg.icipe. org/dataportal/dataset/differential-immune-responses-in-newand-old-fruit-fly-parasitoid-association.International Development Research Centre (IDRC) and the Australian Centre for International Agricultural Research (ACIAR) for the project “Alien invasive fruit flies in Southern Africa: Implementation of a sustainable IPM programme to combat".https://www.frontiersin.org/journals/physiologydm2022Zoology and Entomolog

Friend or foe : symbiotic bacteria in bactrocera dorsalis–parasitoid associations

DATA AVAILABILITY STATEMENT : The datasets generated during and/or analyzed during the current study are available from the corresponding author(s) on reasonable request.Parasitoids are promising biocontrol agents of the devastating fruit fly, Bactrocera dorsalis. However, parasitoid performance is a function of several factors, including host-associated symbiotic bacteria. Providencia alcalifaciens, Citrobacter freundii, and Lactococcus lactis are among the symbiotic bacteria commonly associated with B. dorsalis, and they influence the eco-physiological functioning of this pest. However, whether these bacteria influence the interaction between this pest and its parasitoids is unknown. This study sought to elucidate the nature of the interaction of the parasitoids, Fopius arisanus, Diachasmimorpha longicaudata, and Psyttlia cosyrae with B. dorsalis as mediated by symbiotic bacteria. Three types of fly lines were used: axenic, symbiotic, and bacteria-monoassociated (Lactococcus lactis, Providencia alcalifaciens, and Citrobacter freundii). The suitable stages of each fly line were exposed to the respective parasitoid species and reared until the emergence of adult flies/parasitoids. Thereafter, data on the emergence and parasitoid fitness traits were recorded. No wasps emerged from the fly lines exposed to P. cosyrae. The highest emergence of F. arisanus and D. longicaudata was recorded in the L. lactis fly lines. The parasitoid progeny from the L. lactis and P. alcalifaciens fly lines had the longest developmental time and the largest body size. Conversely, parasitoid fecundity was significantly lower in the L. lactis lines, whereas the P. alcalifaciens lines significantly improved fecundity. These results elucidate some effects of bacterial symbionts on host– parasitoid interactions and their potential in enhancing parasitoid-oriented management strategies against B. dorsalis.The International Development Research Centre (IDRC) and the Australian Centre for International Agricultural Research (ACIAR); the Norwegian Agency for Development Cooperation (NORAD), the Section for Research, Innovation, and Higher Education; the Swedish International Development Cooperation Agency (Sida); the Swiss Agency for Development and Cooperation (SDC); the Australian Centre for International Agricultural Research (ACIAR); the Federal Democratic Republic of Ethiopia; and the Government of the Republic of Kenya.https://www.mdpi.com/journal/biologyam2024Zoology and EntomologySDG-15:Life on lan

Shaping the microbial landscape: parasitoid-driven modifications of Bactrocera dorsalis microbiota

DATA AVAILABILITY : The datasets generated during and/or analyzed during the current study are available in the Sequence Read Archive (SRA) at NCBI under Bioproject: PRJNA1042921.ESM 1 : Online resource 1. Table showing the relative abundance of the bacterial phyla of B. dorsalis larval guts post-parasitisation by Diachasmimorpha longicaudata and Psyttalia cosyrae.ESM 2 : Online resource 2. Table showing the percentage relative abundance of the most common bacterial genera in Bactrocera dorsalis. It includes the unparasitised larvae (control) and those parasitised by Diachasmimorpha longicaudata (BD-DL) and Psyttalia cosyra (BD-PC).ESM 3 : Online resource 3. Relative abundance of selected bacterial genera across the different Bactrocera dorsalis larval groups (Control, parasitized by Diachasmimorpha longicaudata and those parasitized by Psyttalia cosyrae).ESM 4 : Online resource 4. Differential abundance of bacterial ASVs and their taxonomic assignment in Diachasmimorpha longicaudata -parasitised Bactrocera dorsalis larvae compared to the control. Statistical significance of ASVs is assigned at a p-adjusted (padj) value less than 0.05.ESM 5 : Online resource 5. Differential abundance of bacterial ASVs and their taxonomic assignment in Psyttalia cosyrae -parasitised Bactrocera dorsalis larvae compared to the control. Statistical significance of ASVs is assigned at a p-adjusted (padj) value less than 0.05.ESM 6 : Online resource 6. Differential abundance of bacterial ASVs and their taxonomic assignment in Psyttalia cosyrae -parasitised Bactrocera dorsalis larvae compared to those parasitised by Diachasmimorpha longicaudata. Statistical significance of ASVs is assigned at a p-adjusted (padj) value less than 0.05.ESM 7 : Online resource 7. Percentage relative abundance of the most common bacteria genera in female Diachasmimorpha longicaudata and Psyttalia cosyrae.ESM 8 : Online resource 8. Percentage relative abundance of the most common fungal phyla in Bactrocera dorsalis. It includes the unparasitised larvae (control) and those parasitised by Diachasmimorpha longicaudata (BD-DL) and Psyttalia cosyrae (BD-PC).ESM 9 : Online resource 9. Percentage relative abundance of the most common fungal genera in Bactrocera dorsalis. It includes the unparasitised larvae (control) and those parasitised by Diachasmimorpha longicaudata (BD-DL) and Psyttalia cosyrae (BD-PC).Koinobiont endoparasitoids regulate the physiology of their hosts through altering host immuno-metabolic responses, processes which function in tandem to shape the composition of the microbiota of these hosts. Here, we employed 16S rRNA and ITS amplicon sequencing to investigate whether parasitization by the parasitoid wasps, Diachasmimorpha longicaudata (Ashmaed) (Hymenoptera: Braconidae) and Psyttalia cosyrae (Wilkinson) (Hymenoptera: Braconidae), induces gut dysbiosis and differentially alter the gut microbial (bacteria and fungi) communities of an important horticultural pest, Bactrocera dorsalis (Hendel) (Diptera: Tephritidae). We further investigated the composition of bacterial communities of adult D. longicaudata and P. cosyrae to ascertain whether the adult parasitoids and parasitized host larvae share microbial taxa through transmission. We demonstrated that parasitism by D. longicaudata induced significant gut perturbations, resulting in the colonization and increased relative abundance of pathogenic gut bacteria. Some pathogenic bacteria like Stenotrophomonas and Morganella were detected in both the guts of D. longicaudata-parasitized B. dorsalis larvae and adult D. longicaudata wasps, suggesting a horizontal transfer of microbes from the parasitoid to the host. The bacterial community of P. cosyrae adult wasps was dominated by Arsenophonus nasoniae, whereas that of D. longicaudata adults was dominated by Paucibater spp. and Pseudomonas spp. Parasitization by either parasitoid wasp was associated with an overall reduction in fungal diversity and evenness. These findings indicate that unlike P. cosyrae which is avirulent to B. dorsalis, parasitization by D. longicaudata induces shifts in the gut bacteriome of B. dorsalis larvae to a pathobiont-dominated community. This mechanism possibly enhances its virulence against the pest, further supporting its candidacy as an effective biocontrol agent of this frugivorous tephritid fruit fly pest.The German Agency for International Cooperation; the International Development Research Centre (IDRC) and the Australian Centre for International Agricultural Research (ACIAR); the Norwegian Agency for Development Cooperation (NORAD), the Section for Research, Innovation, and Higher Education; the Swedish International Development Cooperation Agency (Sida); the Swiss Agency for Development and Cooperation (SDC); the Australian Centre for International Agricultural Research (ACIAR); the Federal Democratic Republic of Ethiopia; and the Government of the Republic of Kenya. Open access funding provided by University of Pretoria.https://link.springer.com/journal/248hj2024Zoology and EntomologySDG-03:Good heatlh and well-bein