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The Gut Microbiota of Sea Turtles and Its Relationship to Their Phylogenetic History Titus Franciscus Scheelings1* , Robert J

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The Gut Microbiota of Sea Turtles and Its Relationship to Their Phylogenetic History Titus Franciscus Scheelings1* , Robert J Scheelings et al. Animal Microbiome (2020) 2:17 Animal Microbiome https://doi.org/10.1186/s42523-020-00034-8 RESEARCH ARTICLE Open Access Microbial symbiosis and coevolution of an entire clade of ancient vertebrates: the gut microbiota of sea turtles and its relationship to their phylogenetic history Titus Franciscus Scheelings1* , Robert J. Moore2, Thi Thu Hao Van2, Marcel Klaassen3 and Richard D. Reina1 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. Keywords: Evolution, Microbiota, Phylogeny, Sea turtle Background individual. Thus, it has been proposed that animals rep- Residing on and within most metazoan species is a di- resent a vastly intricate biological ‘super organism’ in verse and complex metropolis of microorganisms (vi- which a proportion of the physiological function is de- ruses, bacteria, fungi and protozoans) known collectively rived from microbial activity [5]. The microbiota has as the microbiota and the occupation of higher organ- been shown to be a heritable trait in a range of verte- isms by prokaryotic and eukaryotic colonists has been a brates [6–11], and there is evidence to suggest that its key factor in driving evolution and radiation of life on composition and function is probably influenced by host Earth [1, 2]. Hosts and their microbiotas form a mutual- phylogeny [12, 13], with co-evolution of the host and istic holobiont so intertwined that the amalgamation of microbiota a critical process in shaping metazoan life [3, 4]. these distinct organisms is often referred to as a holo- Ultimately, it appears that a bidirectional interaction of host biome, and their combined genetic material collectively physiology and gut microbiota over evolutionary time is re- defined as the hologenome [3, 4]. This multigenomic sponsible for determining host dietary niche and adaptation microcosm has become so integral to animal homeosta- [12]. Understanding these relationships using a multi- sis that it can no longer be considered separate from the disciplinary approach by combining microbiological tech- niques with phylogenetic analyses, is fundamental to * Correspondence: [email protected] exploring the origins of complex, multicellular organisms. 1 School of Biological Sciences, Monash University, Wellington Rd, Clayton, Investigating closely-related species with clearly defined Victoria 3800, Australia Full list of author information is available at the end of the article phylogenies is extremely informative, because analysis is © The Author(s). 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. Scheelings et al. Animal Microbiome (2020) 2:17 Page 2 of 12 not confounded by vast expanses of evolutionary periods threatened [48]. Marine turtles are highly evolved for a with multiple missing links. Thus, evolutionarily old taxa completely aquatic life, but, like almost all reptiles they with relatively simple phylogenetic histories are highly- are still tied to the terrestrial environment for egg-laying desirable candidates for such an investigation. Sea turtles [14]. The majority of sea turtle species are scattered un- represent an excellent group of species to study in this evenly throughout all three tropical oceans, with the ex- context, because all extant species, including their phyl- ception of the flatback and Kemp’s ridley turtles, which ogeny, are well described [14], and they originate from an have relatively restricted distributions [14]. Additionally, approximately 200 million year old lineage that has gone the leatherback turtle is a more cold adapted species through intermittent periods of slow and intermediate with a more cosmopolitan distribution, and may be evolution and diversification [15], meaning that any de- found occupying waters at higher latitudes than the scribed relationships are robust and profound. Exploring other species [14]. Sea turtle diets vary remarkably over the bidirectional interplay of evolutionary forces acting on life stage, and among species [49]. For example, the lea- the host-microbiota relationship is an important step in therback feeds primarily on gelatinous zooplankton for comprehending the origins of metazoan physiology. its entire existence, while the green turtle is predomin- The major site for microbial inhabitation in animals is ately omnivorous during the oceanic phase of its life, but the gastrointestinal tract, where immense numbers of then undergoes an ontogenic dietary shift to herbivory microorganisms confer myriad beneficial properties to as it transitions to neritic (nearshore) habitats later in their host. These complex interactions are an exciting and life [49], resulting in a discernible shift in the bacterial emerging area of evolutionary biology. Historically, the communities during this phase of their life [33]. Sea tur- importance of microflora to non-human species has pre- tles are unique among the Reptilia, in that they are the dominately focused on their role during digestion, particu- only members that undergo long-distance migrations, ri- larly of complex carbohydrates in herbivorous animals. valling those of other vertebrate species [50], and during However, these investigations have begun to broaden with this time they typically do not forage [51], which may the realisation of the greater role that they play in the have an effect on their microbiota [17, 52–56]. health and ecology of all species [2]. How the microbiota has contributed to the evolution- Investigations into the microbiota of reptiles, including ary history of sea turtles, and the extraordinary physio- sea turtles, are limited to studies describing microbial com- logical adaptations of these species has been little munities [16–29], factors that influence their composition studied, and as a result, we attempted to address this [30–43], and how they affect host physiology [8, 9, 44–46], deficit by examining the microbial populations of the but investigations into the influence of phylogenetic factors world’s sea turtle species. In this investigation we affecting microbiota composition in this taxon are rare. Ir- present the most comprehensive data on the microbiota respective of the potential host-phylogenetic signal in of sea turtles that has been compiled to date. Further- microbiota composition at a broad taxonomic level, it has more, this is one of the most complete microbiota stud- been shown that at a more individual level, diet, captivity, ies to have been conducted in any taxa, because we geography, and feeding regime all influence the microbiota obtained samples from an entire clade of the evolution- [9, 17, 32], and that fermenting bacteria are important for ary tree and we were able to explore some of the phylo- digestion in herbivorous species [47]. genetic relationships that exist between sea turtles and Sea turtles are among the most imperilled species on their microbiotas. The aims of this investigation were to Earth and therefore a deeper understanding of their categorise the microbiota composition of the world’s sea physiology is important to their conservation. The role turtle species, to explore any relationships between sea that microbiota plays in the health, behaviour and physi- turtle phylogeny and microbiota composition, and to ology of humans and animals is undeniable, and its cat- examine how sea turtle microbiotas have changed over egorisation in marine turtles is the next important step evolutionary time. in understanding how these species adapt to a changing environment. There are seven extant species of sea tur- Results tle, the leatherback turtle (Dermochelys coriacea), green Samples were collected from 120 turtles, with sequen- turtle (Chelonia mydas), flatback turtle (Natator depres- cing results obtained in all
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