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

Abstract

Background: The microbiota plays a critical role in host homeostasis and has been shown to be a major driving force in host evolution. However, our understanding of these important relationships is hampered by a lack of data for many species, and by significant gaps in sampling of the evolutionary tree. In this investigation we improve our understanding of the host-microbiome relationship by obtaining samples from all seven extant species of sea turtle, and correlate microbial compositions with host evolutionary history. Results: Our analysis shows that the predominate phyla in the microbiota of nesting sea turtles was Proteobacteria. We also demonstrate a strong relationship between the bacterial phyla SR1 and sea turtle phylogeny, and that sea turtle microbiotas have changed very slowly over time in accordance with their similarly slow phenotypic changes. Conclusions: This is one of the most comprehensive microbiota studies to have been performed in a single clade of animals and further improves our knowledge of how microbial populations have influenced vertebrate evolution.

Microbial communities of wild-captured Kemp’s ridley (Lepidochelys kempii) and green sea turtles (Chelonia mydas)

“…This is the first study to our knowledge to report wild Kemp's ridley turtle microbiomes at this life stage. The only other published study including wild healthy Kemp's ridley turtle microbial communities involves colonic swabs from adult nesting turtles in Mexico (Scheelings et al 2020a). The adult samples were predominately composed of the order Campylobacterales, which were also present in our Kemp's ridley cloaca samples, though the samples diverged at the family level.…”

“…Microbial communities play a role in host development and function, including nutrition, metabolism, immune response, behavior, and sociality (Ley et al 2008b, Amato 2013, McFall-Ngai et al 2013, Bordenstein & Theis 2015, Colston & Jackson 2016. Thus far, studies of sea turtle microbial communities have primarily focused on the gut of loggerhead or green turtles (Abdelrhman et al 2016, Ahasan et al 2017, 2018, Price et al 2017, Campos et al 2018, Biagi et al 2019, Bloodgood et al 2020, McDermid et al 2020, Scheelings et al 2020c, although studies on other species are becoming more common (Samuelson et al 2020, Scheelings et al 2020a. Variations in the cloacal microbiome of green turtles were evident between different habitats (pelagic vs. neritic), which suggests that environmental and dietary factors contribute to microbial community composition in that turtle species (Price et al 2017, Campos et al 2018.…”

“…A more recent study of the gastrointestinal microbiota encompassed all species of sea turtles, but it is difficult to compare across species when all were adult nesting females from different locations in the world (Scheelings et al 2020a). Microbial communities of nesting flatback turtles Natator depressus and loggerhead turtles differ based on populations (Scheelings et al 2020b,c), highlighting that sampling turtles from different geographic regions is still important, but creates limitations in understanding species differences.…”

Fecal Microbiota Characterization of Seychelles Giant Tortoises (Aldabrachelys gigantea) Living in Both Wild and Controlled Environments

“…In contrast, Yuan et al (2015) confirmed the results of the present study, reporting a higher prevalence of Bacteroidetes over Firmicutes in gopher tortoises. Studies on carnivorous reptiles of the Testudines order, such as carnivorous sea turtles, showed that Firmicutes and Bacteroidetes were also the major phyla of their gut microbiota, even though differences in the ratio were present (Abdelrhman et al, 2016;Arizza et al, 2019), presumably due to different diets, climates, habitats or phylogenetic distances (Pluske et al, 1997;Hasan and Yang, 2019;Scheelings et al, 2020).…”

“…To date, several studies have focused on the gut microbiota of mammals, especially that of humans, but also of birds, fish and insects, etc. However, little research on this topic has been carried out on reptiles (Scheelings et al, 2020), and has focused mainly on carnivorous species (Arizza et al, 2019;Biagi et al, 2019), whereas herbivorous reptiles are still underrepresented.…”