Skin and fur bacterial diversity and community structure on American southwestern bats: effects of habitat, geography and bat traits

Winter, Ara S.; Hathaway, Jennifer J.M.; Kimble, Jason C; Buecher, Debbie C.; Valdez, Ernest W.; Porras-Alfaro, Andrea; Young, Jesse M.; Read, Kaitlyn J. H.; Northup, Diana E.

doi:10.7717/peerj.3944

Cited by 27 publications

(23 citation statements)

References 38 publications

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“…behavioral, immune response, and microbiomes), may play a role in WNS susceptibility . While investigations into the microbiomes of North American bats have been conducted to help characterize their skin microbiota (Avena et al, 2016;Lemieux-Labonté, Simard, Willis, & Lapointe, 2017;Winter et al, 2017), host-microbial interactions and their impact on bat health remains an important knowledge gap (Avena et al, 2016). Comparing the bacterial and fungal microbial composition of Pd-positive and Pd-negative bats across the range of Pd spread in North America provides an opportunity to investigate the changes a pathogenic fungus has on the host skin microbial community across several bat species.…”

Section: Introductionmentioning

confidence: 99%

White-nose syndrome restructures bat skin microbiomes

Ange-Stark

Cheng

Hoyt

et al. 2019

Preprint

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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, and Perimyotis 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 ITS amplicon approach. We found that for M. lucifugus, a species that experiences high mortality from white-nose syndrome, bacterial microbiome diversity was dramatically lower when P. destructans is present. Key bacterial families-including those potentially involved in pathogen defense-significantly differed in abundance in bats infected with P. destructans compared to uninfected bats. However, skin bacterial diversity was not lower in E. fuscus or P. subflavus when P. destructans was 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 of P. destructans for 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 WNS in M. lucifugus, but not for other bat species impacted by white-nose syndrome.

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Section: Introductionmentioning

confidence: 99%

White-nose syndrome restructures bat skin microbiomes

Ange-Stark

Cheng

Hoyt

et al. 2019

Preprint

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“…Most studies were performed using Illumina next generation sequencing (targeting the v3-v4 region) (De Mandal et al 2015, Avena et al 2016, Lemieux-Labonté et al 2016, Dietrich et al 2017, Dietrich and Markotter 2019). We chose multi-primer bacterial 16S™ Metagenomics for this study because it targets altogether 7 different hypervariable regions of the 16S rRNA gene (in comparison to previous studies where one or two regions were targeted, such as V1, V2 (Winter et al 2017), V3 and/ or V4 region (Lemieux-Labonté et al 2016, Wilkinson et al 2016). This approach allowed us to get a better overview of the diversity of bacterial communities present (Barb et al 2016).…”

Section: Discussionmentioning

confidence: 99%

“…Also, the same V4 region was studied to determine the gut microbiota and the associated diet of several bat species in the Neotropics (Carrillo-Araujo et al 2015). In other studies, two regions were assess, such as V3 and V4 to determine the bacteria present in bat flies from Madagascar (Wilkinson et al 2016) and from other biological samples (saliva, urine, feces, see Dietrich et al 2017), while the V1-V2 region was targeted to determine the skin and fur microbiome of bats from North America (Winter et al 2017).…”

Section: Discussionmentioning

confidence: 99%

“…On the other hand, studies on bacterial pathogens in bats have been primarily performed using species-specific PCR-based detection tests (Concannon et al 2005, Kamani et al 2014, Cicuttin et al 2017), while metagenomics may be used as a tool to discover new bacteria and viruses that may affect animals and may be transmitted to humans (Blomström et al 2010, Blomström et al 2011, Belák et al 2013, Franco Filho et al, 2019). Studies targeting the bacteriome of bats are a handful and these used samples of excreta (De Mandal et al 2015, Dietrich et al 2015), skin and fur (Avena et al 2016, Lemieux-Labonté et al 2016, Winter et al 2017) or ectoparasites (Wilkinson et al 2016).…”

Section: Introductionmentioning

confidence: 99%

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The heart microbiome of insectivorous bats from Central and South Eastern Europe

Corduneanu

Mihalca

Sándor

et al. 2020

Preprint

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Host associated microbiome not only may affect the individual health-status or provide insights into the species- or group specific bacterial communities but may act as early warning signs in the assessment of zoonotic reservoirs, offering clues to predict, prevent and control possible episodes of emerging zoonoses. Bats may be carriers and reservoirs of multiple pathogens such as viruses, bacteria and parasites, showing in the same time robust immunity against many of them. The microbiota plays a fundamental role on the induction, training and function of the host immune system and the immune system has largely evolved in order to maintain the symbiotic relationship of the host with these diverse microbes. Thus, expanding our knowledge on bat-associated microbiome it can be usefully in understanding bats’ outstanding immune capacities. The aim of this study was to investigate the presence of different bacterial communities in heart tissue of insectivorous bats, Nyctalus noctula, Pipistrellus pipistrellus and Rhinoplophus hipposideros, from Central and Eastern Europe using high-throughput sequencing of variable regions of the 16S rRNA. In addition, species-specific PCRs were used to validate the presence of the vector-borne pathogens Bartonella spp. and Rickettsia spp. In this study we identified a wide variety of bacterial groups, with the most abundant phyla being Proteobacteria and Firmicutes. The results showed that at individual level, the year or location had no effect on the diversity and composition of the microbiome, however host species determined both structure and abundance of the bacterial community. We report the presence of vector-borne bacteria Bartonella spp. in samples of N. noctula and indications of Rickettsia spp. in R. hipposideros. Our results provide a first insight into the bacterial community found in heart tissue of bats from Central and South Eastern Europe.

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“…Finally, we cannot exclude that contamination from the skin and fur of bats may have occurred when collecting urine and feces. Indeed, the microbiota of bat's skin and fur is rich (Avena et al, ; Winter et al, ) and control samples (by swabbing the skin and fur of bats) should therefore be included in future investigations.…”

Section: Discussionmentioning

confidence: 99%

Studying the microbiota of bats: Accuracy of direct and indirect samplings

Dietrich

Markotter

2019

Ecology and Evolution

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Given the recurrent bat‐associated disease outbreaks in humans and recent advances in metagenomics sequencing, the microbiota of bats is increasingly being studied. However, obtaining biological samples directly from wild individuals may represent a challenge, and thus, indirect passive sampling (without capturing bats) is sometimes used as an alternative. Currently, it is not known whether the bacterial community assessed using this approach provides an accurate representation of the bat microbiota. This study was designed to compare the use of direct sampling (based on bat capture and handling) and indirect sampling (collection of bat's excretions under bat colonies) in assessing bacterial communities in bats. Using high‐throughput 16S rRNA sequencing of urine and feces samples from Rousettus aegyptiacus , a cave‐dwelling fruit bat species, we found evidence of niche specialization among different excreta samples, independent of the sampling approach. However, sampling approach influenced both the alpha‐ and beta‐diversity of urinary and fecal microbiotas. In particular, increased alpha‐diversity and more overlapping composition between urine and feces samples was seen when direct sampling was used, suggesting that cross‐contamination may occur when collecting samples directly from bats in hand. In contrast, results from indirect sampling in the cave may be biased by environmental contamination. Our methodological comparison suggested some influence of the sampling approach on the bat‐associated microbiota, but both approaches were able to capture differences among excreta samples. Assessment of these techniques opens an avenue to use more indirect sampling, in order to explore microbial community dynamics in bats.

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Skin and fur bacterial diversity and community structure on American southwestern bats: effects of habitat, geography and bat traits

Cited by 27 publications

References 38 publications

White-nose syndrome restructures bat skin microbiomes

White-nose syndrome restructures bat skin microbiomes

The heart microbiome of insectivorous bats from Central and South Eastern Europe

Studying the microbiota of bats: Accuracy of direct and indirect samplings

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