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1. Mechanisms behind the Madness: How Do Zombie-Making Fungal Entomopathogens Affect Host Behavior To Increase Transmission?

   https://doi.org/10.1128/mBio.01872-21  

   de Bekker, Charissa; Beckerson, William C.; Elya, Carolyn (October 2021, mBio)

   Garsin, Danielle A. (Ed.)

   ABSTRACT Transmission is a crucial step in all pathogen life cycles. As such, certain species have evolved complex traits that increase their chances to find and invade new hosts. Fungal species that hijack insect behaviors are evident examples. Many of these “zombie-making” entomopathogens cause their hosts to exhibit heightened activity, seek out elevated positions, and display body postures that promote spore dispersal, all with specific circadian timing. Answering how fungal entomopathogens manipulate their hosts will increase our understanding of molecular aspects underlying fungus-insect interactions, pathogen-host coevolution, and the regulation of animal behavior. It may also lead to the discovery of novel bioactive compounds, given that the fungi involved have traditionally been understudied. This minireview summarizes and discusses recent work on zombie-making fungi of the orders Hypocreales and Entomophthorales that has resulted in hypotheses regarding the mechanisms that drive fungal manipulation of insect behavior. We discuss mechanical processes, host chemical signaling pathways, and fungal secreted effectors proposed to be involved in establishing pathogen-adaptive behaviors. Additionally, we touch on effectors’ possible modes of action and how the convergent evolution of host manipulation could have given rise to the many parallels in observed behaviors across fungus-insect systems and beyond. However, the hypothesized mechanisms of behavior manipulation have yet to be proven. We, therefore, also suggest avenues of research that would move the field toward a more quantitative future. 

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2. Pathogen-microbiome interactions and the virulence of an entomopathogenic fungus

   https://doi.org/10.1128/aem.02293-23  

   Kolp, Matthew R; de_Anda_Acosta, Yazmin; Brewer, William; Nichols, Holly L; Goldstein, Elliott B; Tallapragada, Keertana; Parker, Benjamin J (June 2024, Applied and Environmental Microbiology)

   Tortosa, Pablo (Ed.)

   ABSTRACT Bacteria shape interactions between hosts and fungal pathogens. In some cases, bacteria associated with fungi are essential for pathogen virulence. In other systems, host-associated microbiomes confer resistance against fungal pathogens. We studied an aphid-specific entomopathogenic fungus calledPandora neoaphidisin the context of both host and pathogen microbiomes. Aphids host several species of heritable bacteria, some of which confer resistance againstPandora. We first found that spores that emerged from aphids that harbored protective bacteria were less virulent against subsequent hosts and did not grow on plate media. We then used 16S amplicon sequencing to study the bacterial microbiome of fungal mycelia and spores during plate culturing and host infection. We found that the bacterial community is remarkably stable in culture despite dramatic changes in pathogen virulence. Last, we used an experimentally transformed symbiont of aphids to show thatPandoracan acquire host-associated bacteria during infection. Our results uncover new roles for bacteria in the dynamics of aphid-pathogen interactions and illustrate the importance of the broader microbiological context in studies of fungal pathogenesis. IMPORTANCEEntomopathogenic fungi play important roles in the population dynamics of many insect species. Understanding the factors shaping entomopathogen virulence is critical for agricultural management and for the use of fungi in pest biocontrol. We show that heritable bacteria in aphids, which confer protection to their hosts against fungal entomopathogens, influence virulence against subsequent hosts. Aphids reproduce asexually and are typically surrounded by genetically identical offspring, and thus these effects likely shape the dynamics of fungal disease in aphid populations. Furthermore, fungal entomopathogens are known to rapidly lose virulence in lab culture, complicating their laboratory use. We show that this phenomenon is not driven by changes in the associated bacterial microbiome. These results contribute to our broader understanding of the aphid model system and shed light on the biology of the Entomophthorales—an important but understudied group of fungi. 

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3. Similarities in the induction of the intracellular pathogen response in Caenorhabditis elegans and the type I interferon response in mammals

   https://doi.org/10.1002/bies.202300097  

   Lažetić, Vladimir; Batachari, Lakshmi E.; Russell, Alistair B.; Troemel, Emily R. (September 2023, BioEssays)

   Abstract Although the type‐I interferon (IFN‐I) response is considered vertebrate‐specific, recent findings about the Intracellular Pathogen Response (IPR) in nematodeCaenorhabditis elegansindicate that there are similarities between these two transcriptional immunological programs. The IPR is induced during infection with natural intracellular fungal and viral pathogens of the intestine and promotes resistance against these pathogens. Similarly, the IFN‐I response is induced by viruses and other intracellular pathogens and promotes resistance against infection. Whether the IPR and the IFN‐I response evolved in a divergent or convergent manner is an unanswered and exciting question, which could be addressed by further studies of immunity against intracellular pathogens inC. elegansand other simple host organisms. Here we highlight similar roles played by RIG‐I‐like receptors, purine metabolism enzymes, proteotoxic stressors, and transcription factors to induce the IPR and IFN‐I response, as well as the similar consequences of these defense programs on organismal development. 

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4. Leveraging machine learning to uncover multi-pathogen infection dynamics across co-distributed frog families

   https://doi.org/10.7717/peerj.18901  

   Wiley, Daniele_L F; Omlor, Kadie N; Torres_López, Ariadna S; Eberle, Celina M; Savage, Anna E; Atkinson, Matthew S; Barrow, Lisa N (January 2025, PeerJ)

   BackgroundAmphibians are experiencing substantial declines attributed to emerging pathogens. Efforts to understand what drives patterns of pathogen prevalence and differential responses among species are challenging because numerous factors related to the host, pathogen, and their shared environment can influence infection dynamics. Furthermore, sampling across broad taxonomic and geographic scales to evaluate these factors poses logistical challenges, and interpreting the roles of multiple potentially correlated variables is difficult with traditional statistical approaches. In this study, we leverage frozen tissues stored in natural history collections and machine learning techniques to characterize infection dynamics of three generalist pathogens known to cause mortality in frogs. MethodsWe selected 12 widespread and abundant focal taxa within three ecologically distinct, co-distributed host families (Bufonidae, Hylidae, and Ranidae) and sampled them across the eastern two-thirds of the United States of America. We screened and quantified infection loadsviaquantitative PCR for three major pathogens: the fungal pathogenBatrachochytrium dendrobatidis(Bd), double-stranded viruses in the lineageRanavirus(Rv), and the alveolate parasite currently referred to as Amphibian Perkinsea (Pr). We then built balanced random forests (RF) models to predict infection status and intensity based on host taxonomy, age, sex, geography, and environmental variables and to assess relative variable importance across pathogens. Lastly, we used one-way analyses to determine directional relationships and significance of identified predictors. ResultsWe found approximately 20% of individuals were infected with at least one pathogen (231 single infections and 25 coinfections). The most prevalent pathogen across all taxonomic groups was Bd (16.9%; 95% CI [14.9–19%]), followed by Rv (4.38%; 95% CI [3.35–5.7%]) and Pr (1.06%; 95% CI [0.618–1.82%]). The highest prevalence and intensity were found in the family Ranidae, which represented 74.3% of all infections, including the majority of Rv infection points, and had significantly higher Bd intensities compared to Bufonidae and Hylidae. Host species and environmental variables related to temperature were key predictors identified in RF models, with differences in importance among pathogens and host families. For Bd and Rv, infected individuals were associated with higher latitudes and cooler, more stable temperatures, while Pr showed trends in the opposite direction. We found no significant differences between sexes, but juvenile frogs had higher Rv prevalence and Bd infection intensity compared to adults. Overall, our study highlights the use of machine learning techniques and a broad sampling strategy for identifying important factors related to infection in multi-host, multi-pathogen systems. 

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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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