Biotic and abiotic factors influencing channel catfish egg and gut microbiome dynamics during early life stages

Razak, Shairah Abdul; Griffin, Matt J.; Mischke, Charles C.; Bosworth, Brian G.; Waldbieser, Geoffrey C.; Wise, David J.; Marsh, Terence L.; Scribner, Kim T.

doi:10.1016/j.aquaculture.2018.08.073

Cited by 19 publications

(17 citation statements)

References 39 publications

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“…Results suggest that the aquatic community that eggs were exposed to during the fertilization and incubation periods was important in determining the taxonomic structure, assembly, and successional change on the egg surfaces. Data are consistent with our previous research with Lake Sturgeon and Channel Catfish Ictalurus punctatus that also revealed that colonization by egg‐associated microbial communities is not random but is influenced by water microbial community composition (Fujimoto et al 2013; Abdul‐Razak et al 2019).…”

Section: Discussionsupporting

confidence: 92%

Effects of Water Filtration and Temperature on Microbial Colonization and Survival of Lake Sturgeon Eggs

2020

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Physical and biotic factors that affect development and survival during the embryonic period of fish are major concerns in aquaculture, particularly when individuals are produced using natural surface water sources. We quantified the effects of bacterial community taxonomic composition and abundance, water filtration treatment, and incubation temperature on the development and survival of embryos from Lake Sturgeon Acipenser fulvescens, a threatened Great Lakes fish species. Eggs were fertilized and incubated using a two‐by‐two treatment design by manipulating water treatments (treated [filtered and UV treated] and untreated stream water) and temperature (12°C and 18°C) during incubation. Egg samples from five full‐sibling families were exposed to each rearing treatment. At different stages during development, eggs were analyzed for egg surface microbial community composition and abundance using terminal restriction fragment length polymorphism methods based on the 16S rRNA gene and quantitative PCR, respectively. Sanger sequencing identified egg‐associated microbial taxa. Microbial community composition derived from terminal restriction fragment length polymorphism was visualized using principal component analysis. Permutational multivariate analysis of variance revealed that the composition of microbial communities that developed on egg surfaces varied as a function of water filtration and temperature. Quantitative PCR analysis revealed that significantly higher microbial abundance was present on surfaces of eggs reared in untreated stream water than on those reared in treated stream water. Temperature did not affect egg surface microbial abundance. Significantly higher egg mortality was documented for eggs reared in unfiltered stream water (mean ± SD = 77.4 ± 17.6%) than for eggs reared in treated stream water (50.3 ± 14.7%). Temperature during incubation did not affect levels of egg mortality. Sequence analysis revealed that certain microbial taxa were associated with eggs characterized by higher survival, including Acidovorax spp. and Massilia spp., suggesting that they may be candidates for natural probiotics. Filtration and UV treatment of surface water was an effective method for modification of egg microbial community composition and quantity and significantly reduced egg mortality.

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Section: Discussionsupporting

confidence: 92%

Effects of Water Filtration and Temperature on Microbial Colonization and Survival of Lake Sturgeon Eggs

2020

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“…ing fish with different feeding habits revealed that Proteobacteria and Firmicutes were the dominant phyla in all fish species (47). Another cross-sectional gut microbiota study performed on channel catfish also indicated the prevalence of Proteobacteria in fish at the earlier stage and the appearance of Firmicutes along with Proteobacteria when the fish reached 65 dph (48) or when the fish were stocked into a nursery pond (11).…”

Section: Figmentioning

confidence: 94%

Ecological and Ontogenetic Components of Larval Lake Sturgeon Gut Microbiota Assembly, Successional Dynamics, and Ecological Evaluation of Neutral Community Processes

Razak

Scribner

2020

Appl Environ Microbiol

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Gastrointestinal (GI) or gut microbiotas play essential roles in host development and physiology. These roles are influenced partly by the microbial community composition. During early developmental stages, the ecological processes underlying the assembly and successional changes in host GI community composition are influenced by numerous factors, including dispersal from the surrounding environment, age-dependent changes in the gut environment, and changes in dietary regimes. However, the relative importance of these factors to the gut microbiota is not well understood. We examined the effects of environmental (diet and water sources) and host early ontogenetic development on the diversity of and the compositional changes in the gut microbiota of a primitive teleost fish, the lake sturgeon (Acipenser fulvescens), based on massively parallel sequencing of the 16S rRNA gene. Fish larvae were raised in environments that differed in water source (stream versus filtered groundwater) and diet (supplemented versus nonsupplemented Artemia fish). We quantified the gut microbial community structure at three stages (prefeeding and 1 and 2 weeks after exogenous feeding began). The diversity declined and the community composition differed significantly among stages; however, only modest differences associated with dietary or water source treatments were documented. Many taxa present in the gut were over- or underrepresented relative to neutral expectations in each sampling period. The findings indicate dynamic relationships between the gut microbiota composition and host gastrointestinal physiology, with comparatively smaller influences being associated with the rearing environments. Neutral models of community assembly could not be rejected, but selectivity associated with microbe-host GI tract interactions through early ontogenetic stages was evident. The results have implications for sturgeon conservation and aquaculture production specifically and applications of microbe-based management in teleost fish generally. IMPORTANCE We quantified the effects of environment (diet and water sources) and host early ontogenetic development on the diversity of and compositional changes in gut microbial communities based on massively parallel sequencing of the 16S rRNA genes from the GI tracts of larval lake sturgeon (Acipenser fulvescens). The gut microbial community diversity declined and the community composition differed significantly among ontogenetic stages; however, only modest differences associated with dietary or water source treatments were documented. Selectivity associated with microbe-host GI tract interactions through early ontogenetic stages was evident. The results have implications for lake sturgeon and early larval ecology and survival in their natural habitat and for conservation and aquaculture production specifically, as well as applications of microbe-based management in teleost fish generally.

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“…(Kraft & Angert, 2017). Microbial communities in the sediment and in dietary items consumed by sturgeon are likely to be more abundant and taxonomically different during the later (warmer) period when late‐spawning females are present (Abdul Razak et al., 2019; Bucci et al., 2014; Hullar et al., 2006). DNA metabarcoding (e.g., Abdul Razak et al., 2019) could be a profitable avenue of research along with quantitative PCR to ascertain changes in dietary microbial community composition and taxonomic abundance in directions consistent with microbial taxa known to produce or degrade thiamine.…”

Section: Discussionmentioning

confidence: 99%

Egg lipid and thiamine vary between early and late spawning lake sturgeon

et al. 2021

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Summary Nutritional deficiency associated with reduced thiamine (vitamin B1) and reduced natural reproduction of salmonid species in the Great Lake Region is well established. The negative relationship between egg thiamine and lipid concentration to post‐hatch larval growth and survival in teleost species, coupled with the limited research of egg thiamine in Acipenseriform species of conservation concern, including lake sturgeon, indicates that study of thiamine concentrations lake sturgeon eggs is warranted. Eggs were collected from females (N = 12) during the early and late portion of the spawning run in 2007 in a wild population from Black Lake, MI. Concentrations of thiamine, lipid and fatty acid concentration were measured along with female biological information (body size and egg size) and characteristics of larvae at hatch. Significant differences in egg thiamine concentrations were observed between early‐ and late‐spawning females (mean ± SD: 2.36 nmol·g−1 ± 1.09 vs. 0.73 ± 0.25 nmol·g−1, W = 0.05, p < .01). No significant relationships were observed between female body size or egg size and egg lipid or thiamine concentration. Differences in lipid and thiamine concentrations were not predictive of larval body size or yolk sac volume at hatch. Total and phosphorylated thiamine were correlated with n‐3 polyunsaturated fatty acids, suggesting that dietary items were likely partially responsible for provisioning of essential compounds. Given the negative effects of low egg thiamine concentration on larval survival in other fish species globally, results indicate that further research in areas of nutrient acquisition and thiamine effects on larval survival, natural recruitment, and hatchery feeding strategies is warranted for lake sturgeon.

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Biotic and abiotic factors influencing channel catfish egg and gut microbiome dynamics during early life stages

Cited by 19 publications

References 39 publications

Effects of Water Filtration and Temperature on Microbial Colonization and Survival of Lake Sturgeon Eggs

Effects of Water Filtration and Temperature on Microbial Colonization and Survival of Lake Sturgeon Eggs

Ecological and Ontogenetic Components of Larval Lake Sturgeon Gut Microbiota Assembly, Successional Dynamics, and Ecological Evaluation of Neutral Community Processes

Egg lipid and thiamine vary between early and late spawning lake sturgeon

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