Geography, Host Genetics, and Cross‐Domain Microbial Networks Structure the Skin Microbiota of Fragmented Brazilian Atlantic Forest Frog Populations

Belasen, Anat M.; Riolo, Michael L.; Bletz, Molly C.; Lyra, Mariana L.; Toledo, Luı́s Felipe; James, Timothy Y.

doi:10.1002/ece3.7594

Cited by 13 publications

(13 citation statements)

References 77 publications

(132 reference statements)

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“…Previous studies have shown that spatial variation has an influence on skin bacterial diversity of terrestrial salamanders [ 14 , 41 , 64 ]; for example populations of Ensatina eschscholtzii from different geographic locations vary in bacterial community composition [ 15 ]. In this study we found that sampling location significantly influences skin bacterial diversity, and this effect is stronger in pre-metamorphic axolotls.…”

Section: Discussionmentioning

confidence: 99%

The skin microbiota of the axolotl Ambystoma altamirani is highly influenced by metamorphosis and seasonality but not by pathogen infection

et al. 2022

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Background Microbiomes have been increasingly recognized as major contributors to host health and survival. In amphibians, bacterial members of the skin microbiota protect their hosts by inhibiting the growth of the fungal pathogen Batrachochytrium dendrobatidis (Bd). Even though several studies describe the influence of biotic and abiotic factors over the skin microbiota, it remains unclear how these symbiotic bacterial communities vary across time and development. This is particularly relevant for species that undergo metamorphosis as it has been shown that host physiology and ecology drastically influence diversity of the skin microbiome. Results We found that the skin bacterial communities of the axolotl A. altamirani are largely influenced by the metamorphic status of the host and by seasonal variation of abiotic factors such as temperature, pH, dissolved oxygen and conductivity. Despite high Bd prevalence in these samples, the bacterial diversity of the skin microbiota did not differ between infected and non-infected axolotls, although relative abundance of particular bacteria were correlated with Bd infection intensity. Conclusions Our work shows that metamorphosis is a crucial process that shapes skin bacterial communities and that axolotls under different developmental stages respond differently to environmental seasonal variations. Moreover, this study greatly contributes to a better understanding of the factors that shape amphibian skin microbiota, especially in a largely underexplored group like axolotls (Mexican Ambystoma species).

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Section: Discussionmentioning

confidence: 99%

The skin microbiota of the axolotl Ambystoma altamirani is highly influenced by metamorphosis and seasonality but not by pathogen infection

et al. 2022

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“…The bacteriome is only a portion of host-associated microbial communities, with protists, multicellular fungi, viruses, archaea, and microscopic metazoans also often in great abundances [ 82 – 85 ]. Microbial assemblages also exist in a complex mucosal substrate that includes host-produced antimicrobial peptides [ 86 , 87 ].…”

Section: Discussionmentioning

confidence: 99%

“…Microbial assemblages also exist in a complex mucosal substrate that includes host-produced antimicrobial peptides [ 86 , 87 ]. These additional components of host skin communities interact with host-associated bacteria [ 84 , 85 ] and may also independently interact with invading microbes [ 86 , 87 ], suggesting that analysis at the level of the entire chemical and biological mucosal matrix may be necessary to fully evaluate Bd resistance mechanisms in H. binotatus . Immunogenetic variation is another factor that could not only help to explain host variation in microbiome assembly [ 85 , 88 , 89 ], but could also contribute to Bd resistance independently of the microbiome [ 37 , 38 , 90 , 91 ].…”

Section: Discussionmentioning

confidence: 99%

Signatures of functional bacteriome structure in a tropical direct-developing amphibian species

et al. 2022

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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 microbe Batrachochytrium 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 in Ischnocnema henselii but no Bd detections in Haddadus binotatus. Haddadus binotatus carried 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 in H. binotatus, which could guide microbiome manipulation as a conservation strategy to protect diverse radiations of direct-developing species from Bd-induced population collapses.

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“…Instead, most research has focussed on speci c fungal pathogen species, such as susceptibility to Batrachochytrium dendrobatidis infection in amphibians [51][52][53]. Few studies have looked at the in uence of MHC variation on wider host-associated fungal communities [54,55]. One study on the Thoropa taophora frog skin microbiome demonstrated that MHC genotype was signi cantly associated with differences in the composition of host-associated microeukaryote communities [54].…”

Section: Introductionmentioning

confidence: 99%

“…Few studies have looked at the in uence of MHC variation on wider host-associated fungal communities [54,55]. One study on the Thoropa taophora frog skin microbiome demonstrated that MHC genotype was signi cantly associated with differences in the composition of host-associated microeukaryote communities [54]. However, as far as we are aware, there are no studies investigating the relationship between MHC variation and host-associated fungal communities in the GM.…”

Section: Introductionmentioning

confidence: 99%

Assessing the causes and consequences of gut mycobiome variation in a wild vertebrate population

Worsley

Davies

Mannarelli

et al. 2022

Preprint

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Background Considerable research has focussed on the importance of bacterial communities within the vertebrate gut microbiome (GM). However, studies investigating the significance of other microbial kingdoms, such as fungi, are notably lacking, despite their potential to influence host processes. Here, we characterise the fungal GM of individuals living in a natural population of Seychelles warblers (Acrocephalus sechellensis). We evaluate the extent to which fungal GM structure is shaped by environment and host factors, including genome-wide heterozygosity and variation at key immune genes (Major histocompatibility Complex (MHC) and Toll-like receptor (TLR) genes). Importantly, we also explore the relationship between fungal GM differences and subsequent host survival. To our knowledge, this is the first time that the genetic drivers and fitness consequences of fungal GM variation have been characterised for a wild vertebrate population. Results Environmental factors, including season and territory quality, explain the largest proportion of variance in the fungal GM. In contrast, neither host age, sex, genome-wide heterozygosity, or TLR3 genotype were associated with fungal GM differences in Seychelles warblers. However, the presence of four MHC-I alleles and one MHC-II allele were associated with changes in fungal GM alpha diversity. Changes in fungal richness ranged from between 1 and 10 sequencing variants lost or gained; in some cases, this accounted for 20% of the fungal variants carried by an individual. In addition to this, overall MHC-I allelic diversity was associated with small, but potentially important, changes in fungal GM composition. This is evidenced by the fact that fungal GM composition differed between individuals that survived or died within seven months of being sampled. Conclusions Our results suggest that environmental factors play a primary role in shaping the fungal GM, but that components of the host immune system – specifically the MHC – may also contribute to variation in fungal communities across individuals within wild populations. Furthermore, variation in the fungal GM can be associated with differential survival in the wild. Further work is needed to establish the causality of such relationships and, thus, the extent to which components of the GM may impact upon host evolution.

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Geography, Host Genetics, and Cross‐Domain Microbial Networks Structure the Skin Microbiota of Fragmented Brazilian Atlantic Forest Frog Populations

Cited by 13 publications

References 77 publications

The skin microbiota of the axolotl Ambystoma altamirani is highly influenced by metamorphosis and seasonality but not by pathogen infection

The skin microbiota of the axolotl Ambystoma altamirani is highly influenced by metamorphosis and seasonality but not by pathogen infection

Signatures of functional bacteriome structure in a tropical direct-developing amphibian species

Assessing the causes and consequences of gut mycobiome variation in a wild vertebrate population

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