Dataset Information

The Behavior of Amphibians Shapes Their Symbiotic Microbiomes.

ABSTRACT: Seasonal dynamics in symbiotic microbiomes have been investigated in a number of vertebrates and are mainly caused by changes in the diet (in the gut microbiome) or the living environment (in the skin microbiome). Most amphibian microbiome studies focus on the skin, whereas internal microbiome structure and dynamics are often overlooked. The present study investigated the seasonal dynamics in three types of symbiotic microbiomes (the skin, stomach, and gut) across four wild frog species, belonging to different families, in May and October. The frogs harbored more water source microbes in May than in October. On the contrary, the frogs harbored more soil source microbes in October than in May. The frog species investigated tend to live in a water environment in May to maintain body surface humidity at high environmental temperatures and to breed. In October, these four species prefer to live on the land, as the environmental temperature decreases, to prepare for hibernation in caves or under stones. Thus, seasonal changes in the wild amphibian symbiotic microbiome may be caused by the difference in microbe transmission from their living environment due to specific behaviors. This study demonstrated that the behavior and living environment of wild amphibians shape their symbiotic microbiome externally (on the skin) and internally (in the stomach and gut). We revealed the potential association between specific behaviors in poikilothermic animals and host symbiotic microbiomes.IMPORTANCE Understanding the interactions between host behavior and microbiome dynamics remains an outstanding priority in the field of microbial ecology. Here, we provide the reader with a simple example of how the behavior and living environment of wild amphibians shape their symbiotic microbiome externally (on the skin) and internally (in the stomach and gut).

SUBMITTER: Xu L

PROVIDER: S-EPMC7394361 | biostudies-literature | 2020 Jul

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

The Behavior of Amphibians Shapes Their Symbiotic Microbiomes.

Xu Liangliang L Xiang Mengmeng M Zhu Wei W Zhang Mengjie M Chen Hua H Huang Jin J Chen Youhua Y Chang Qing Q Jiang Jianping J Zhu Lifeng L

mSystems 20200728 4

Seasonal dynamics in symbiotic microbiomes have been investigated in a number of vertebrates and are mainly caused by changes in the diet (in the gut microbiome) or the living environment (in the skin microbiome). Most amphibian microbiome studies focus on the skin, whereas internal microbiome structure and dynamics are often overlooked. The present study investigated the seasonal dynamics in three types of symbiotic microbiomes (the skin, stomach, and gut) across four wild frog species, belongi ...[more]

PMID: 32723798

Similar Datasets

Project description:Amphibians possess beneficial skin bacteria that protect against the disease chytridiomycosis by producing secondary metabolites that inhibit the pathogen Batrachochytrium dendrobatidis (Bd). Metabolite production may be a mechanism of competition between bacterial species that results in host protection as a by-product. We expect that some co-cultures of bacterial species or strains will result in greater Bd inhibition than mono-cultures. To test this, we cultured four bacterial isolates (Bacillus sp., Janthinobacterium sp., Pseudomonas sp. and Chitinophaga arvensicola) from red-backed salamanders (Plethodon cinereus) and cultured isolates both alone and together to collect their cell-free supernatants (CFS). We challenged Bd with CFSs from four bacterial species in varying combinations. This resulted in three experimental treatments: (1) CFSs of single isolates; (2) combined CFSs of two isolates; and (3) CFSs from co-cultures. Pair-wise combinations of four bacterial isolates CFSs were assayed against Bd and revealed additive Bd inhibition in 42.2% of trials, synergistic inhibition in 42.2% and no effect in 16.6% of trials. When bacteria isolates were grown in co-cultures, complete Bd inhibition was generally observed, and synergistic inhibition occurred in four out of six trials. A metabolite profile of the most potent co-culture, Bacillus sp. and Chitinophaga arvensicola, was determined with LC-MS and compared with the profiles of each isolate in mono-culture. Emergent metabolites appearing in the co-culture were inhibitory to Bd, and the most potent inhibitor was identified as tryptophol. Thus mono-cultures of bacteria cultured from red-backed salamanders interacted synergistically and additively to inhibit Bd, and such bacteria produced emergent metabolites when cultured together, with even greater pathogen inhibition. Knowledge of how bacterial species interact to inhibit Bd can be used to select probiotics to provide amphibians with protection against Bd.

Project description:Many female squids and cuttlefishes have a symbiotic reproductive organ called the accessory nidamental gland (ANG) that hosts a bacterial consortium involved with egg defense against pathogens and fouling organisms. While the ANG is found in multiple cephalopod families, little is known about the global microbial diversity of these ANG bacterial symbionts. We used 16S rRNA gene community analysis to characterize the ANG microbiome from different cephalopod species and assess the relationship between host and symbiont phylogenies. The ANG microbiome of 11 species of cephalopods from four families (superorder: Decapodiformes) that span seven geographic locations was characterized. Bacteria of class Alphaproteobacteria, Gammaproteobacteria, and Flavobacteriia were found in all species, yet analysis of amplicon sequence variants by multiple distance metrics revealed a significant difference between ANG microbiomes of cephalopod families (weighted/unweighted UniFrac, Bray-Curtis, P = 0.001). Despite being collected from widely disparate geographic locations, members of the family Sepiolidae (bobtail squid) shared many bacterial taxa including (~50%) Opitutae (Verrucomicrobia) and Ruegeria (Alphaproteobacteria) species. Furthermore, we tested for phylosymbiosis and found a positive correlation between host phylogenetic distance and bacterial community dissimilarity (Mantel test r = 0.7). These data suggest that closely related sepiolids select for distinct symbionts from similar bacterial taxa. Overall, the ANGs of different cephalopod species harbor distinct microbiomes and thus offer a diverse symbiont community to explore antimicrobial activity and other functional roles in host fitness.IMPORTANCEMany aquatic organisms recruit microbial symbionts from the environment that provide a variety of functions, including defense from pathogens. Some female cephalopods (squids, bobtail squids, and cuttlefish) have a reproductive organ called the accessory nidamental gland (ANG) that contains a bacterial consortium that protects eggs from pathogens. Despite the wide distribution of these cephalopods, whether they share similar microbiomes is unknown. Here, we studied the microbial diversity of the ANG in 11 species of cephalopods distributed over a broad geographic range and representing 15-120 million years of host divergence. The ANG microbiomes shared some bacterial taxa, but each cephalopod species had unique symbiotic members. Additionally, analysis of host-symbiont phylogenies suggests that the evolutionary histories of the partners have been important in shaping the ANG microbiome. This study advances our knowledge of cephalopod-bacteria relationships and provides a foundation to explore defensive symbionts in other systems.

Project description:BackgroundOne of the most charismatic, and yet not completely resolved example of mutualistic interaction is the partnership of clownfish and its symbiotic sea anemone. The mechanism explaining this tolerance currently relies on the molecular mimicry of clownfish epithelial mucus, which could serve as camouflage, preventing the anemone's nematocysts' discharge. Resident bacteria are known as key drivers of epithelial mucus chemical signature in vertebrates. A recent study has proposed a restructuration of the skin microbiota in a generalist clown fish when first contacting its symbiotic anemone. We explored a novel hypothesis by testing the effect of remote interaction on epithelial microbiota restructuration in both partners.MethodsWith metataxonomics, we investigated the epithelial microbiota dynamic of 18 pairs of percula clownfish (Amphiprion percula) and their symbiotic anemone Heteractis magnifica in remote interaction, physical interaction and control groups for both partners during a 4-week trial.ResultsThe Physical and Remote Interaction groups' results evidence gradual epithelial microbiota convergence between both partners when fish and anemone were placed in the same water system. This convergence occurred preceding any physical contact between partners, and was maintained during the 2-week interaction period in both contact groups. After the interaction period, community structure of both fish and anemone's epthelial community structures maintained the interaction signature 2 weeks after fish-anemone pairs' separation. Furthermore, the interaction signature persistence was observed both in the Physical and Remote Interaction groups, thus suggesting that water-mediated chemical communication between symbiotic partners was strong enough to shift the skin microbiota durably, even after the separation of fish-anemone pairs. Finally, our results suggest that fish-anemone convergent microbiota restructuration was increasingly associated with the parallel recruitment of three Flavobacteriaceae strains closely related to a tyrosinase-producing Cellulophaga tyrosinoxydans.ConclusionsOur study shows that bacterial community restructuration, in the acclimation process, does not only rely on direct physical contact. Furthermore, our results challenge, for the first time, the traditional unidirectional chemical camouflage hypothesis, as we argue that convergence of the epithelial microbiota of both partners may play essential roles in establishing mutual acceptance. Video abstract Fish-anemone symbiotic relationship.

Dataset Information

The Behavior of Amphibians Shapes Their Symbiotic Microbiomes.

Publications

The Behavior of Amphibians Shapes Their Symbiotic Microbiomes.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets