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.