Host‐associated bacterial community succession during amphibian development

Abstract

Amphibians undergo significant developmental changes during their life cycle, as they typically move from a primarily aquatic environment to a more terrestrial one. Amphibian skin is a mucosal tissue that assembles communities of symbiotic microbiota. However, it is currently not well understood as to where amphibians acquire their skin symbionts, and whether the sources of microbial symbionts change throughout development. In this study, we utilized data collected from four wild boreal toad populations (Anaxyrus boreas); specifically, we sampled the skin bacterial communities during toad development, including eggs, tadpoles, subadults and adults as well as environmental sources of bacteria (water, aquatic sediment and soil). Using 16S rRNA marker gene profiling coupled with SourceTracker, we show that while primary environmental sources remained constant throughout the life cycle, secondary sources of boreal toad symbionts significantly changed with development. We found that toad skin communities changed predictably across development and that two developmental disturbance events (egg hatching and metamorphosis) dictated major changes. Toad skin communities assembled to alternative stable states following each of these developmental disturbances. Using the predicted average rRNA operon copy number of the communities at each life stage, we showed how the skin bacterial communities undergo a successional pattern whereby "fast-growing" (copiotroph) generalist bacteria dominate first before "slow-growing" (oligotroph) specialized bacteria take over. Our study highlights how host-associated bacterial community assembly is tightly coupled to host development and that host-associated communities demonstrate successional patterns akin to those observed in free-living bacteria as well as macrofaunal communities.

Introduction: The host‐associated microbiome: Pattern, process and function

“…They demonstrate a complete reorganization of the microbial community during this time, with major shifts corresponding to hatching of eggs and tadpole metamorphosis. At each stage of development, there is also general succession of microbiota from copiotrophic (organisms that thrive in high nutrient conditions) to oligotrophic (those common in low nutrient conditions) taxa, which, they argue, supports a scenario of initial colonization by opportunistic taxa followed by replacement with competitive dominants (Prest, Kimball, Kueneman, & McKenzie, ). By comparing amphibian communities to those in the environment, they also show that colonizing microbes are predominately coming from pond water throughout development (Prest et al., ).…”

“…At each stage of development, there is also general succession of microbiota from copiotrophic (organisms that thrive in high nutrient conditions) to oligotrophic (those common in low nutrient conditions) taxa, which, they argue, supports a scenario of initial colonization by opportunistic taxa followed by replacement with competitive dominants (Prest, Kimball, Kueneman, & McKenzie, 2018). By comparing amphibian communities to those in the environment, they also show that colonizing microbes are predominately coming from pond water throughout development (Prest et al, 2018). That different communities are assembled over time from the same environmental pool demonstrates how changes in the host impose a varying habitat filter, favouring different colonizers as they acquire their microbiota anew each life cycle stage.…”

Probiotics as a tool for disease mitigation in wildlife: insights from food production and medicine

“…86 Furthermore, the skin communities undergo a predictable succession pattern following metamorphosis, akin to the way a community responds to disturbance. 87 Therefore, we view the developmental window after metamorphosis as a potentially optimal time for probiotic application, when the skin bacterial communities are reassembling. Metamorphic stage amphibians are also a good target for probiotic treatments, because they are highly abundant (during late summer), such that many can be collected for probiotic treatment, and they are often highly vulnerable to chytridiomycosis.…”

“…[82][83][84] Amphibians undergo a complete metamorphosis that can lead to large changes in their gut and skin bacterial communities. 85,86 In particular, amphibian skin bacteria are lost during metamorphosis as the skin sheds, 87 and a new community of bacteria assembles on the metamorphicstaged individuals. This may be viewed as an opportune time for beneficial bacteria to become established while there is more open niche space on the skin.…”

Editorial 2019

“…The second section featured a number of manuscripts that investigated the structure of the microbiome in an attempt to understand the drivers of microbiota community assembly and turnover. Some contributions weighed in on the role of host phylogeny vs. ecology (Erlandson, Savage, Wei, Cavender‐Bares, & Peay, ; Ivens, Gadau, Kiers, & Kronauer, 2018; Hernandez‐Gomez, Briggler, & Williams, ; Kohl, Dearing, & Bordenstein, ; Nishida & Ochman, ; Roth‐Schulze et al., ; Schuelke, Pereira, Hardy, & Bik, ), others probed how the presence of hosts themselves alters the microbiota around them (Chen & Parfrey, ; Shukla, Vogel, Heckel, Vilcinskas, & Kaltenpoth, ), one investigated patterns of co‐infection (Rock et al, ) and one documented changes in microbiota during development (Prest, Kimball, Kueneman, & McKenzie, ). A few studies in this section studied the structure of the microbiome with manipulative experiments (e.g., Chen & Parfrey, ; Erlandson et al, ; Morella, Gomez, Wang, Leung, & Koskella, ; Raymann, Bobay, & Moran, ).…”