skip to main content


Title: Parental care contributes to vertical transmission of microbes in a skin-feeding and direct-developing caecilian
Abstract Background

Our current understanding of vertebrate skin and gut microbiomes, and their vertical transmission, remains incomplete as major lineages and varied forms of parental care remain unexplored. The diverse and elaborate forms of parental care exhibited by amphibians constitute an ideal system to study microbe transmission, yet investigations of vertical transmission among frogs and salamanders have been inconclusive. In this study, we assess bacteria transmission inHerpele squalostoma,an oviparous direct-developing caecilian in which females obligately attend juveniles that feed on their mother’s skin (dermatophagy).

Results

We used 16S rRNA amplicon-sequencing of the skin and gut of wild caughtH. squalostomaindividuals (males, females, including those attending juveniles) as well as environmental samples. Sourcetracker analyses revealed that juveniles obtain an important portion of their skin and gut bacteria communities from their mother. The contribution of a mother’s skin to the skin and gut of her respective juveniles was much larger than that of any other bacteria source. In contrast to males and females not attending juveniles, only the skins of juveniles and their mothers were colonized by bacteria taxa Verrucomicrobiaceae, Nocardioidaceae, and Erysipelotrichaceae. In addition to providing indirect evidence for microbiome transmission linked to parental care among amphibians, our study also points to noticeable differences between the skin and gut communities ofH. squalostomaand that of many frogs and salamanders, which warrants further investigation.

Conclusion

Our study is the first to find strong support for vertical bacteria transmission attributed to parental care in a direct-developing amphibian species. This suggests that obligate parental care may promote microbiome transmission in caecilians.

 
more » « less
Award ID(s):
1845634
NSF-PAR ID:
10413664
Author(s) / Creator(s):
; ; ; ;
Publisher / Repository:
Springer Science + Business Media
Date Published:
Journal Name:
Animal Microbiome
Volume:
5
Issue:
1
ISSN:
2524-4671
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract Background

    Host microbiomes may differ under the same environmental conditions and these differences may influence susceptibility to infection. Amphibians are ideal for comparing microbiomes in the context of disease defense because hundreds of species face infection with the skin-invading microbeBatrachochytrium dendrobatidis(Bd), and species richness of host communities, including their skin bacteria (bacteriome), may be exceptionally high. We conducted a landscape-scale Bd survey of six co-occurring amphibian species in Brazil’s Atlantic Forest. To test the bacteriome as a driver of differential Bd prevalence, we compared bacteriome composition and co-occurrence network structure among the six focal host species.

    Results

    Intensive sampling yielded divergent Bd prevalence in two ecologically similar terrestrial-breeding species, a group with historically low Bd resistance. Specifically, we detected the highest Bd prevalence inIschnocnema henseliibut no Bd detections inHaddadus binotatus.Haddadus binotatuscarried the highest bacteriome alpha and common core diversity, and a modular network partitioned by negative co-occurrences, characteristics associated with community stability and competitive interactions that could inhibit Bd colonization.

    Conclusions

    Our findings suggest that community structure of the bacteriome might drive Bd resistance inH. binotatus, which could guide microbiome manipulation as a conservation strategy to protect diverse radiations of direct-developing species from Bd-induced population collapses.

     
    more » « less
  2. Background Insects are the most diverse group of animals which have established intricate evolutionary interactions with bacteria. However, the importance of these interactions is still poorly understood. Few studies have focused on a closely related group of insect species, to test the similarities and differences between their microbiota. Heliconius butterflies are a charismatic recent insect radiation that evolved the unique ability to use pollen as a protein source, which affected life history traits and resulted in an elevated speciation rates. We hypothesize that different Heliconius butterflies sharing a similar trophic pollen niche, harbor a similar gut flora within species, population and sexes. Methods To test our hypothesis, we characterized the microbiota of 38 adult male and female butterflies representing six species of Heliconius butterflies and 2 populations of the same species. We sequenced the V4 region of the 16S rRNA gene with the Roche 454 system and analyzed the data with standard tools for microbiome analysis. Results Overall, we found a low microbial diversity with only 10 OTUs dominating across all individuals, mostly Proteobacteria and Firmicutes, which accounted for  99.5% of the bacterial reads. When rare reads were considered, we identified a total of 406 OTUs across our samples. We identified reads within Phyla Chlamydiae , found in 5 butterflies of four species. Interestingly, only three OTUs were shared among all 38 individuals ( Bacillus, Enterococcus and Enterobacteriaceae ). Altogether, the high individual variation overshadowed species and sex differences. Thus, bacterial communities were not structured randomly with 13% of beta-diversity explained by species, and 40 rare OTUs being significantly different across species. Finally, 13 OTUs, including the intercellular symbiont Spiroplasma, varied significantly in relative abundance between males and females. Discussion The Heliconius microbial communities in these 38 individuals show a low diversity with few differences in the rare microbes between females, males, species or populations. Indeed, Heliconius butterflies, similarly to other insects, are dominated by few OTUs, mainly from Proteobacteria and Firmicutes. The overall low microbial diversity observed contrasts with the high intra-species variation in microbiome composition. This could indicate that much of the microbiome maybe acquired from their surroundings. The significant differences between species and sexes were restricted to rare taxa, which could be important for microbial community stability under changing conditions as seen in other host-microbiome systems. The presence of symbionts like Spiroplasma or Chlamydiae , identified in this study for the first time in Heliconius , could play a vital role in their behavior and evolution by vertical transmission. Altogether, our study represents a step forward into the description of the microbial diversity in a charismatic group of closely related butterflies. 
    more » « less
  3. ABSTRACT

    Host-associated microbial communities can influence physiological processes of macroorganisms, including contributing to infectious disease resistance. For instance, some bacteria that live on amphibian skin produce antifungal compounds that inhibit two lethal fungal pathogens, Batrachochytrium dendrobatidis (Bd) and Batrachochytrium salamandrivorans (Bsal). Therefore, differences in microbiome composition among host species or populations within a species can contribute to variation in susceptibility to Bd/Bsal. This study applies 16S rRNA sequencing to characterize the skin bacterial microbiomes of three widespread terrestrial salamander genera native to the western United States. Using a metacommunity structure analysis, we identified dispersal barriers for these influential bacteria between salamander families and localities. We also analysed the effects of habitat characteristics such as percent natural cover and temperature seasonality on the microbiome. We found that certain environmental variables may influence the skin microbial communities of some salamander genera more strongly than others. Each salamander family had a somewhat distinct community of putative anti-Bd skin bacteria, suggesting that salamanders may select for a functional assembly of cutaneous symbionts that could differ in its ability to protect these amphibians from disease. Our observations raise the need to consider host identity and environmental heterogeneity during the selection of probiotics to treat wildlife diseases.

     
    more » « less
  4. Abstract

    The amphibian skin microbiome has been the focus of numerous studies because of the protective effects that some bacteria provide against the pathogenic fungus Batrachochytrium dendrobatidis, which has caused a global panzootic among amphibians. However, the mechanisms driving community structure and function in the amphibian skin microbiome are still poorly understood, and longitudinal analyses of the skin microbiome have not yet been conducted in wild populations. In this study, we investigate longitudinal patterns in the skin microbiome of 19 individually marked adult frogs from two wild populations of the endangered Sierra Nevada yellow-legged frog (Rana sierrae), sampled over the course of 2 years. We found that individuals with low bacterial diversity (dominated by order Burkhorderiales) had significantly more stable bacterial communities than those with higher diversity. Amplicon sequence variants (ASVs) with high relative abundance were significantly less transient than those with low relative abundance, and ASVs with intermediate-level relative abundances experienced the greatest volatility over time. Based on these results, we suggest that efforts to develop probiotic treatments to combat B. dendrobatidis should focus on bacteria that are found at high relative abundances in some members of a population, as these strains are more likely to persist and remain stable in the long term.

     
    more » « less
  5. Abstract

    Because microbes use carotenoids as an antioxidant for protection, dietary carotenoids could be associated with gut microbiota composition. We aimed to determine associations among reported carotenoid intake, plasma carotenoid concentrations, and fecal bacterial communities in pregnant women. Pregnant women (n= 27) were enrolled in a two‐arm study designed to assess feasibility of biospecimen collection and delivery of a practical nutrition intervention. Plasma and fecal samples were collected and women were surveyed with a 24‐hr dietary checklist and recalls. Plasma carotenoids were analyzed by HPLC using photodiode array detection. Fecal bacteria were analyzed by 16S rRNA DNA sequencing. Results presented are cross‐sectional from the 36‐week gestational study visit combined across both study arms due to lack of significant differences between intervention and usual care groups (n= 23 women with complete data). Recent intake of carotenoid‐containing foods included carrots, sweet potatoes, mangos, apricots, and/or bell peppers for 48% of women; oranges/orange juice (17%); egg (39%); tomato/tomato‐based sauces (52%); fruits (83%); and vegetables (65%). Average plasma carotenoid concentrations were 6.4 µg/dL α‐carotene (AC), 17.7 µg/dL β‐carotene (BC), 11.4 µg/dL cryptoxanthin, 39.0 µg/dL trans‐lycopene, and 29.8 µg/dL zeaxanthin and lutein. AC and BC concentrations were higher in women who recently consumed foods high in carotenoids. CR concentrations were higher in women who consumed oranges/orange juice. Microbiota α‐diversity positively correlated with AC and BC. Microbiota β‐diversity differed significantly across reported intake of carotenoid containing foods and plasma concentrations of AC. This may reflect an effect of high fiber or improved overall dietary quality, rather than a specific effect of carotenoids.

    Practical Application

    Little is known about the association between the gut microbiome and specific dietary microconstituents, such as carotenoids, especially during pregnancy. This research demonstrates that a carotenoid‐rich diet during pregnancy supports a diverse microbiota, which could be one mechanism by which carotenoids promote health.

     
    more » « less