Keywords: Teratoscincus roborowskii, seasonal dietary changes, gut microbiota, metabolomics, ecological adaptation
Introduction
The intestinal structure of animals satisfies the requirements of food digestion and nutrient absorption. It also maintains homeostasis of gut microbes (Sommer & Bäckhed, 2013). Complex interactions of the gut microbial ecosystem occur between the host and its gut microbes (McFall-Ngai et al., 2013). The gut microbiota plays an important role in the intestinal immune system, energy metabolism (Sommer & Bäckhed, 2013), reproductive activity (MacLeod et al., 2022), and longevity (Kim & Benayoun, 2020)of the host.
The composition, structure, and function of gut microbiota are influenced by multiple factors (Suzuki & Worobey, 2014). Seasonal environmental fluctuations can significantly alter the gut microbiota of animals. For example, the gut microbiota of Pteromys volansoriivaries seasonally on an ecological scale (Liu et al., 2019). In addition, seasonal physiological changes associated with hibernation also alter gut microbiota in greater horseshoe bats (Rhinolophus ferrumequinum ) and brown bears (Ursus arctos ) (Sommer et al., 2016; Xiao et al., 2019). Trophic niche expansion is an active adjustment of wildlife to seasonal and environmental changes (Guisan et al., 2014), and dietary shifts can affect or even determine the composition of animal gut microbes that change dynamically with the season (Maurice et al., 2015). Studies on wood mice (Apodemus sylvaticus ), plateau pikas (Ochotona curzoniae ), brown frogs (Fejervarya limnocharis ), black howler monkeys (Alouatta pigra ), and giant pandas (Ailuropoda melanoleuca ) have shown that gut microbes undergo dynamic seasonal changes (Maurice et al., 2015; Fan et al., 2022; Huang et al., 2021; Amato et al., 2015; Wu et al., 2017). These results indicate that seasonal dietary shifts can significantly alter animal gut microbiota.
At present, fecal metabolomics is widely considered a key tool for studying the relationship between hosts and their gut microbiota and has attracted extensive attention (Zierer et al., 2018). Metabolomics enables researchers to identify a large proportion of the metabolites present in a sample. By analyzing these products of cellular metabolism, metabolomics can reveal valuable information about an organism’s metabolic or physiological state at the time of sampling (Tang et al., 2020). For example, in wildlife research, joint analysis of metabolomics and gut microbiota has revealed differences in the abundance and metabolic phenotypes of gut microbes of Panthera pardus japonensis in captive and wild environments (Hua et al., 2020). The co-metabolic patterns of the gut and microbes in mountain gorillas (Gorilla beringei beringei ) and western lowland gorillas (Gorilla gorilla ) indicate that dietary restriction is a potential factor driving specific changes in gut microbes (Gomez et al., 2016). Combined analysis of gut microbes and metabolomics has also become an effective approach for identifying relevant biomarkers to reveal complex changes in metabolic and biochemical pathways (Tran et al., 2020).
Significant differences in the composition, structure, and abundance of gut microbiota in different animal groups, such as mammals (Zhao et al., 2018), birds (Grond et al., 2018), and fishes (Egerton et al., 2018), have been extensively studied. Reptiles, especially lizards, have a special evolutionary history and environmental adaptation behaviors (Pianka & Vitt, 2003). however, relatively little research has been conducted on the gut microbes of lizards (Colston & Jackson, 2016). Relevant studies have focused on changes in the patterns of gut microbes of crocodile lizards (Shinisaurus crocodilurus ), western fence lizards (Sceloporus occidentalis ), northern grass lizards (Takydromus septentrionalis ), and mesquite lizards (Sceloporus grammicus ) under the influence of human activities, temperature, diet, altitude, and other factors (Tang et al., 2020; Moeller et al., 2020; Zhou et al., 2020; Montoya-Ciriaco et al., 2020).
The Turpan wonder gecko (Teratoscincus roborowskii ) is a walking gecko species endemic to the Turpan Depression in the Xinjiang Uyghur Autonomous Region of China (Shi et al., 2007; Shi et al., 2002). They live in extreme desert environments (Song et al., 2009; Zhou et al., 2019). Research on Turpan wonder geckos mainly focuses on foraging mode, activity rhythms, and seed dispersal (Song et al., 2017; Werner et al., 1997; Yang et al., 2021). Field observations and dietary analysis have shown that T. roborowskii feeds mainly on insects in spring, whereas the proportion of caper fruits in the food can reach 85% in summer and autumn, showing a significant seasonal shift in dietary habits (Liu et al., 2010; Yang et al., 2021). This seasonal dietary shift may be an important factor in T. roborowskii adaptation to harsh and arid desert habitats.
The Turpan wonder gecko goes through a long hibernation process every year (Li et al., 2010). Fruit-eating strategies are more likely to be deployed with seasonal variations in food availability to maximize pre-hibernation food intake and satisfy nutritional requirements (Naya et al., 2010; Robbins et al., 2012). Related studies have shown that switching from insects to plant fruits is a common mechanism through which migrating birds accumulate fat for energy (Marshall et al., 2016). Gerbils (Psammomys obesus ), which also live in a desert environment, can convert a small amount of carbohydrates into endogenous fructose due to the stimulation of a high-salt diet, thereby aggravating the tendency to obesity and effectively adapting to the lack of food (Kaiser et al., 2012). Turpan wonder geckos face abundant caper fruit resources in summer and autumn. From this, we can speculate that fresh caper fruit is not only an excellent source of water and nutrients but also a special way for Turpan wonder geckos to acquire energy and store fat during the pre-hibernation period. This dramatic shift in seasonal dietary habits can lead to alterations in gut microbes to meet the functional needs of dietary transition. Therefore, 16S rRNA sequencing technology and LC-MS metabolomics were used in this study to explore changes in the gut microbiota and metabolic patterns of Turpan wonder geckos during spring and autumn.