The effect of diet on the gastrointestinal microbiome of juvenile rehabilitating green turtles (Chelonia mydas)

Abstract

Threatened and endangered green turtles (Chelonia mydas) are unique because as juveniles they recruit from pelagic to near-shore waters and shift from an omnivorous to primarily herbivorous diet (i.e. seagrass and algae). Nevertheless, when injured and ill animals are admitted to rehabilitation, animal protein (e.g. seafood) is often offered to combat poor appetite and emaciation. We examined how the fecal microbiome of juvenile green turtles changed in response to a dietary shift during rehabilitation. We collected fecal samples from January 2014-January 2016 from turtles (N = 17) in rehabilitation at the Georgia Sea Turtle Center and used next generation sequencing to analyze bacterial community composition. Samples were collected at admission, mid-rehabilitation, and recovery, which entailed a shift from a mixed seafood-vegetable diet at admission to a primarily herbivorous diet at recovery. The dominant phyla changed over time, from primarily Firmicutes (55.0%) with less Bacteroidetes (11.4%) at admission, to primarily Bacteroidetes (38.4%) and less Firmicutes (31.8%) at recovery. While the microbiome likely shifts with the changing health status of individuals, this consistent inversion of Bacteroidetes and Firmicutes among individuals likely reflects the increased need for protein digestion, for which Bacteroidetes are important. Firmicutes are significant in metabolizing plant polysaccharides; thus, fewer Firmicutes may result in underutilization of wild diet items in released individuals. This study demonstrates the importance of transitioning rehabilitating green turtles to an herbivorous diet as soon as possible to afford them the best probability of survival.

Comparative Analysis of the Fecal Microbiota of Wild and Captive Beal’s Eyed Turtle (Sacalia bealei) by 16S rRNA Gene Sequencing

“…This pattern was also seen in turtle studies, with herbivorous species having gut microbiota dominated by Firmicutes (Gaillard, 2014;Modica, 2016;Fugate et al, 2019;Peng et al, 2020), while carnivorous and omnivorous species had gut microbiotas dominated by Bacteroidetes (Biagi et al, 2018;Bloodgood et al, 2020). In particular, Bloodgood et al (2020) showed that gut microbial diversity has the ability to change in relation to diet; when herbivorous green sea turtles (Chelonia mydas) were given an omnivorous diet (seafood + vegetables) in captivity, their gut microbiota shifted from being dominated by Firmicutes to Bacteriodetes. In our study, the proportion of Bacteroidetes was higher in captive S. bealei (12.37 ± 11.97% in WS, 24.94 ± 19.62% in CS), as well as Firmicutes (18.12 ± 13.65% in WS, 68.61 ± 22.97% in CS).…”

“…A trend first found in humans, individuals with plant-based diets have gut microbiota dominated by taxa in the phylum Firmicutes that metabolize plant polysaccharides and degrade cellulose into volatile fatty acids, while animal-based diets are dominated by taxa in the phyla Proteobacteria that are bile tolerant (David et al, 2014). This pattern was also seen in turtle studies, with herbivorous species having gut microbiota dominated by Firmicutes (Gaillard, 2014;Modica, 2016;Fugate et al, 2019;Peng et al, 2020), while carnivorous and omnivorous species had gut microbiotas dominated by Bacteroidetes (Biagi et al, 2018;Bloodgood et al, 2020). In particular, Bloodgood et al (2020) showed that gut microbial diversity has the ability to change in relation to diet; when herbivorous green sea turtles (Chelonia mydas) were given an omnivorous diet (seafood + vegetables) in captivity, their gut microbiota shifted from being dominated by Firmicutes to Bacteriodetes.…”

“…Studies of turtle gut microbial diversity have found influences of diet (Modica, 2016;Bloodgood et al, 2020), geography (Butterfield, 2019), and ontogeny (Yuan et al, 2015;Peng et al, 2020). For the influence of diet, the pattern in turtles was similar to that seen in humans; individuals with plant-based diets had gut microbiota dominated by Firmicutes, while individuals with animal-based diets had gut microbiota dominated by Bacteroidetes (David et al, 2014).…”

“…Turtles are particularly poorly represented in the gut microbiota literature, but the available studies suggest the gut microbiota is influenced by diet, geography, and ontogeny. For diet, turtle groups with different ecologies (sea turtles, freshwater turtles, tortoises) show a similar trend; species with plant-based diets had gut microbiota dominated by the bacterial phylum Firmicutes (Gaillard, 2014;Modica, 2016;Fugate et al, 2019;Peng et al, 2020), while species with animal-based diets were dominated by Bacterioidetes (Biagi et al, 2018;Bloodgood et al, 2020). In this study, we focus on the freshwater Beal's eyed turtle (Sacalia bealei) from southern China (Anhui, Fujian, Guangdong, Guangxi, Guizhou, and Jiangxi Provinces, and Hong Kong) (Shi et al, 2008).…”

Microbial symbiosis and coevolution of an entire clade of ancient vertebrates: the gut microbiota of sea turtles and its relationship to their phylogenetic history

“…Investigations into the microbiota of reptiles, including sea turtles, are limited to studies describing microbial communities [16][17][18][19][20][21][22][23][24][25][26][27][28][29], factors that influence their composition [30][31][32][33][34][35][36][37][38][39][40][41][42][43], and how they affect host physiology [8,9,[44][45][46], but investigations into the influence of phylogenetic factors affecting microbiota composition in this taxon are rare. Irrespective of the potential host-phylogenetic signal in microbiota composition at a broad taxonomic level, it has been shown that at a more individual level, diet, captivity, geography, and feeding regime all influence the microbiota [9,17,32], and that fermenting bacteria are important for digestion in herbivorous species [47].…”