Effects of host genetics and environment on egg‐associated microbiotas in brown trout (Salmo trutta)

Abstract

Recent studies found fish egg-specific bacterial communities that changed over the course of embryogenesis, suggesting an interaction between the developing host and its microbiota. Indeed, single-strain infections demonstrated that the virulence of opportunistic bacteria is influenced by environmental factors and host immune genes. However, the interplay between a fish embryo host and its microbiota has not been studied yet at the community level. To test whether host genetics affects the assemblage of egg-associated bacteria, adult brown trout (Salmo trutta) were sampled from a natural population. Their gametes were used for full-factorial in vitro fertilizations to separate sire from dam effects. In total, 2520 embryos were singly raised under experimental conditions that differently support microbial growth. High-throughput 16S rRNA amplicon sequencing was applied to characterize bacterial communities on milt and fertilized eggs across treatments. Dam and sire identity influenced embryo mortality, time until hatching and composition of egg-associated microbiotas, but no link between bacterial communities on milt and on fertilized eggs could be found. Elevated resources increased embryo mortality and modified bacterial communities with a shift in their putative functional potential. Resource availability did not significantly affect any parental effects on embryo performance. Sire identity affected bacterial diversity that turned out to be a significant predictor of hatching time: embryos associated with high bacterial diversity hatched later. We conclude that both host genetics and the availability of resources define diversity and composition of egg-associated bacterial communities that then affect the life history of their hosts.

Succession of embryonic and the intestinal bacterial communities of Atlantic salmon (Salmo salar) reveals stage‐specific microbial signatures

“…The transition from eyed eggs (EE) to those prior to hatching (EBH) was characterized based on changes in both richness and phylogenetic diversity as well as the composition, particularly at the genus level: Methylotenera and Methylophilus were dominant in the EE, whereas Undibacterium was dominant in the EBH and HL groups. Previous reports have not clearly described the presence and biological functions of these genera on fish eggs though Methylotenera has been found abundant on the brown trout ( Salmo trutta ) embryos (Wilkins, Fumagalli, & Wedekind, ). The abovementioned communities of the phylum Proteobacteria are likely to be egg surface‐specific (Fujimoto, Crossman, Scribner, & Marsh, ; Llewellyn et al., ; Yoshimizu, Kimura, & Sakai, ) and the mechanisms causing the shift in the genera are not clear yet, although neutral and nonneutral assembly models have been proposed for zebrafish (Burns et al., ).…”

Environmental stress linked to consumption of maternally derived carotenoids in brown trout embryos (Salmo trutta)

“…See Wilkins et al. () for the corresponding analysis of the influence of treatment, dam, sire, and bacterial diversity on embryo survival, hatching timing, and bacterial diversity within these 56 half‐sib families. Here, we include these survival data into the larger sample (126 half‐sib families in total) in order to test for correlations to carotenoids.…”

“…We reared the resulting embryos singly until hatching at different levels of organic pollution that create stressful environments for the embryos (Jacob et al., ; Wedekind, Gessner, Vazquez, Maerki, & Steiner, ). Adding nutrient broth to brown trout embryos has been shown to increase embryo mortality, change the egg‐associated bacterial community composition, and cause a transition in their functional gene pathways (Wilkins, Fumagalli, & Wedekind, ). Increased mortality rates in nutrient broth‐treated embryos could even be linked to a lower allelic diversity in their immune system (major histocompatibility complex; Jacob et al., ).…”

Early life stress causes persistent impacts on the microbiome of Atlantic salmon

“…In the case of the acute stress during late embryogenesis, it is probable that exposure to iced water directly affected microbial communities associated with the egg shell, and thus the subsequent assembly of the gut and skin microbiome. The egg shell microbiome is extremely diverse and known to be directly influenced by the chemical and physical characteristics of the surrounding water, including temperature (Liu et al 2014; Wilkins et al 2016). Upon hatching, these microbial communities are the primary colonisers of the fish intestine and skin and therefore fundamentally influence successive community structure (Stephens et al 2016; Wilkins et al 2016).…”

“…The egg shell microbiome is extremely diverse and known to be directly influenced by the chemical and physical characteristics of the surrounding water, including temperature (Liu et al 2014; Wilkins et al 2016). Upon hatching, these microbial communities are the primary colonisers of the fish intestine and skin and therefore fundamentally influence successive community structure (Stephens et al 2016; Wilkins et al 2016). Differences in microbial colonisation history can alter the availability of ecological niches for successive colonisers, and can explain lasting differences in community assembly in otherwise identical environmental conditions (Fukami 2015; Sprockett et al 2018; Walter & Ley 2011).…”