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1. Aphid facultative symbionts confer no protection against the fungal entomopathogen Batkoa apiculata

   https://doi.org/10.1371/journal.pone.0286095  

   Inchauregui, Rose A.; Tallapragada, Keertana; Parker, Benjamin J. (May 2023, PLOS ONE)

   Sanda, Nafiu Bala (Ed.)

   Fungi in the familyEntomophthoraceaeare prevalent pathogens of aphids. Facultative symbiotic bacteria harbored by aphids, includingSpiroplasma sp. andRegiella insecticola, have been shown to make their hosts more resistant to infection with the fungal pathogenPandora neoaphidis. How far this protection extends against other species of fungi in the familyEntomophthoraceaeis unknown. Here we isolated a strain of the fungal pathogenBatkoa apiculatainfecting a natural population of pea aphids (Acyrthosiphon pisum) and confirmed its identity by sequencing the 28S rRNA gene. We then infected a panel of aphids each harboring a different species or strain of endosymbiotic bacteria to test whether aphid symbionts protect againstB.apiculata. We found no evidence of symbiont-mediated protection against this pathogen, and our data suggest that some symbionts make aphids more susceptible to infection. This finding is relevant to our understanding of this important model of host-microbe interactions, and we discuss our results in the context of aphid-microbe ecological and evolutionary dynamics. 

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2. An aphid symbiont confers protection against a specialized RNA virus, another increases vulnerability to the same pathogen

   https://doi.org/10.1111/mec.16801  

   Higashi, Clesson H.; Nichols, William L.; Chevignon, Germain; Patel, Vilas; Allison, Suzanne E.; Kim, Kyungsun Lee; Strand, Michael R.; Oliver, Kerry M. (February 2023, Molecular Ecology)

   Abstract Insects often harbour heritable symbionts that provide defence against specialized natural enemies, yet little is known about symbiont protection when hosts face simultaneous threats. In pea aphids (Acyrthosiphon pisum), the facultative endosymbiontHamiltonella defensaconfers protection against the parasitoid,Aphidius ervi, andRegiella insecticolaprotects against aphid‐specific fungal pathogens, includingPandora neoaphidis. Here, we investigated whether these two common aphid symbionts protect against a specialized virusA. pisum virus(APV), and whether their antifungal and antiparasitoid services are impacted by APV infection. We found that APV imposed large fitness costs on symbiont‐free aphids and these costs were elevated in aphids also housingH. defensa. In contrast, APV titres were significantly reduced and costs to APV infection were largely eliminated in aphids withR. insecticola. To our knowledge,R. insecticolais the first aphid symbiont shown to protect against a viral pathogen, and only the second arthropod symbiont reported to do so. In contrast, APV infection did not impact the protective services of eitherR. insecticolaorH. defensa. To better understand APV biology, we produced five genomes and examined transmission routes. We found that moderate rates of vertical transmission, combined with horizontal transfer through food plants, were the major route of APV spread, although lateral transfer by parasitoids also occurred. Transmission was unaffected by facultative symbionts. In summary, the presence and species identity of facultative symbionts resulted in highly divergent outcomes for aphids infected with APV, while not impacting defensive services that target other enemies. These findings add to the diverse phenotypes conferred by aphid symbionts, and to the growing body of work highlighting extensive variation in symbiont‐mediated interactions. 

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3. Heritable viral symbionts in the family Iflaviridae are widespread among aphids

   https://doi.org/10.1101/2025.02.03.636351  

   Rozo-Lopez, Paula; Torres, Vanesa; Torres, Joseph; Käfer, Simon; Parker, Benjamin J (February 2025, bioRxiv)

   A<sc>bstract</sc> Heritable microbes shape host phenotypes and are important drivers of evolution. While interactions between insects and bacterial symbionts have been extensively studied, the prevalence and consequences of insect-viral symbiosis are an open question. We show that viral symbionts in the familyIflaviridaeare widespread among aphids, an important model for research on bacterial symbiosis. We discovered multiple new species of iflaviruses that are maintained in asexual lines without apparent fitness costs and are transmitted vertically from mothers to offspring. Using field data and phylogenetic evidence, we further show that aphid iflaviruses likely move horizontally across species, but through laboratory experiments, we demonstrated that horizontal transfer among species infesting the same host plants does not persist throughout clonal lineages. Using quantitative PCR and immunohistochemistry, we discovered that viral infections localize in the host fat bodies and developing embryos. Surprisingly, we also found viral infections inside bacteria-housing cells called bacteriocytes, with a positive correlation between viral and bacterial symbiont density, indicating a mechanism for vertical transmission. Together, our work suggests that iflaviruses are an important but previously unrecognized piece of aphid symbiosis and sets the stage to use this model to answer new questions about host-microbe associations. I<sc>mportance</sc>In recent years, the rise of metatranscriptome sequencing has led to the rapid discovery of novel viral sequences in insects. However, few studies have carefully investigated the dynamics of insect-virus interactions to produce a general understanding of viral symbiosis. Aphids are a significant agricultural pest but also an important model for understanding the evolution of host-microbe interactions and the molecular basis of bacterial symbiosis. We show that heritable iflaviruses are an important but previously unrecognized part of the aphid heritable microbiome, with viral symbionts transmitted alongside bacteria from mothers to offspring, potentially via specialized bacteriocytes that house symbiotic microbes. Our findings have important implications for furthering the understanding of insect-microbe symbiosis and the potential for biocontrol of agriculturally relevant pest species. 

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4. Bacterial and fungal components of the gut microbiome have distinct, sex-specific roles in Hawaiian Drosophila reproduction

   https://doi.org/10.1101/2023.07.14.549088  

   Medeiros, Matthew J; Seo, Laura; Macias, Aziel; Price, Donald K; Yew, Joanne Y (July 2023, bioRxiv)

   Abstract Gut microbiomes provide numerous physiological benefits for host animals. The role of bacterial members of microbiomes in host physiology is well-documented. However, much less is known about the contributions and interactions of fungal members of the microbiome even though fungi are significant components of many microbiomes, including those of humans and insects. Here, we used antibacterial and antifungal drugs to manipulate the gut microbiome of a Hawaiian picture-wingDrosophilaspecies,D. grimshawi, and identified distinct, sex-specific roles for the bacteria and fungi in microbiome community stability and reproduction. Female oogenesis, fecundity and mating drive were significantly diminished when fungal communities were suppressed. By contrast, male fecundity was more strongly affected by bacterial but not fungal populations. For males and females, suppression of both bacteria and fungi severely reduced fecundity and altered fatty acid levels and composition, implicating the importance of interkingdom interactions on reproduction and lipid metabolism. Overall, our results reveal that bacteria and fungi have distinct, sexually-dimorphic effects on host physiology and interkingdom dynamics in the gut help to maintain microbiome community stability and enhance reproduction. 

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5. White-nose syndrome restructures bat skin microbiomes

   https://doi.org/10.1128/spectrum.02715-23  

   Ange-Stark, Meghan; Parise, Katy L; Cheng, Tina L; Hoyt, Joseph R; Langwig, Kate E; Frick, Winifred F; Kilpatrick, A Marm; Gillece, John; MacManes, Matthew D; Foster, Jeffrey T (December 2023, Microbiology Spectrum)

   Ding, Xia (Ed.)

   ABSTRACT The skin microbiome is an essential line of host defense against pathogens, yet our understanding of microbial communities and how they change when hosts become infected is limited. We investigated skin microbial composition in three North American bat species (Myotis lucifugus,Eptesicus fuscus, andPerimyotis subflavus) that have been impacted by the infectious disease, white-nose syndrome, caused by an invasive fungal pathogen,Pseudogymnoascus destructans. We compared bacterial and fungal composition from 154 skin swab samples and 70 environmental samples using a targeted 16S rRNA and internal transcribed spacer amplicon approach. We found that forM. lucifugus, a species that experiences high mortality from white-nose syndrome, bacterial microbiome diversity was dramatically lower whenP. destructanswas present. Key bacterial families—including those potentially involved in pathogen defense—significantly differed in abundance in bats infected withP. destructanscompared to uninfected bats. However, skin bacterial diversity was not lower inE. fuscusorP. subflavuswhenP. destructanswas present despite populations of the latter species declining sharply from white-nose syndrome. The fungal species present on bats substantially overlapped with the fungal taxa present in the environment at the site where the bat was sampled, but fungal community composition was unaffected by the presence ofP. destructansfor any of the three bat species. This species-specific alteration in bat skin bacterial microbiomes after pathogen invasion may suggest a mechanism for the severity of white-nose syndrome inM. lucifugusbut not for other bat species impacted by the disease. IMPORTANCEInherent complexities in the composition of microbiomes can often preclude investigations of microbe-associated diseases. Instead of single organisms being associated with disease, community characteristics may be more relevant. Longitudinal microbiome studies of the same individual bats as pathogens arrive and infect a population are the ideal experiment but remain logistically challenging; therefore, investigations like our approach that are able to correlate invasive pathogens to alterations within a microbiome may be the next best alternative. The results of this study potentially suggest that microbiome-host interactions may determine the likelihood of infection. However, the contrasting relationship between Pd and the bacterial microbiomes ofMyotis lucifugusandPerimyotis subflavusindicate that we are just beginning to understand how the bat microbiome interacts with a fungal invader such as Pd. 

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