The Bamboo-Eating Giant Panda Harbors a Carnivore-Like Gut Microbiota, with Excessive Seasonal Variations

Abstract

The giant panda evolved from omnivorous bears. It lives on a bamboo-dominated diet at present, but it still retains a typical carnivorous digestive system and is genetically deficient in cellulose-digesting enzymes. To find out whether this endangered mammalian species, like other herbivores, has successfully developed a gut microbiota adapted to its fiber-rich diet, we conducted a 16S rRNA gene-based large-scale structural profiling of the giant panda fecal microbiota. Forty-five captive individuals were sampled in spring, summer, and late autumn within 1 year. Significant intraindividual variations in the diversity and structure of gut microbiota across seasons were observed in this population, which were even greater than the variations between individuals. Compared with published data sets involving 124 gut microbiota profiles from 54 mammalian species, these giant pandas, together with 9 captive and 7 wild individuals investigated previously, showed extremely low gut microbiota diversity and an overall structure that diverged from those of nonpanda herbivores but converged with those of carnivorous and omnivorous bears. The giant panda did not harbor putative cellulose-degrading phylotypes such as Ruminococcaceae and Bacteroides bacteria that are typically enriched in other herbivores, but instead, its microbiota was dominated by Escherichia/Shigella and Streptococcus bacteria. Members of the class Clostridia were common and abundant in the giant panda gut microbiota, but most of the members present were absent in other herbivores and were not phylogenetically related with known cellulolytic lineages. Therefore, the giant panda appears not to have evolved a gut microbiota compatible with its newly adopted diet, which may adversely influence the coevolutionary fitness of this herbivore. IMPORTANCEThe giant panda, an endangered mammalian species endemic to western China, is well known for its unique bamboo diet. Unlike other herbivores that have successfully evolved anatomically specialized digestive systems to efficiently deconstruct fibrous plant matter, the giant panda still retains a gastrointestinal tract typical of carnivores. We characterized the fecal bacterial communities from a giant panda population to determine whether this animal relies on its symbiotic gut microbiota to cope with the complex carbohydrates that dominate its diet, as is common in other herbivores. We found that the giant panda gut microbiota is low in diversity and highly variable across seasons. It also shows an overall composition typical of bears and entirely differentiated from other herbivores, with low levels of putative cellulose-digesting bacteria. The gut microbiota of this herbivore, therefore, may not have well adapted to its highly fibrous diet, suggesting a potential link with its poor digestive efficiency.

Characterizing the microbiota in gastrointestinal tract segments of Rhabdophis subminiatus: Dynamic changes and functional predictions

“…In addition, several factors play key roles in shaping the composition of an animal's gut microbiota, including diet, host phylogeny, gut morphology, and geographical environment (Ley, Lozupone, Hamady, Knight, & Gordon, ). Previous studies have shown that carnivorous, herbivorous, and omnivorous animals have different gut microbiota compositions (Ley, Hamady, et al, ; Xue et al, ). The gastrointestinal tract (GIT) of carnivorous animals is relatively simple compared to those of omnivores and herbivores (Schwab & Gänzle, ; Xue et al, ).…”

“…Previous studies have shown that carnivorous, herbivorous, and omnivorous animals have different gut microbiota compositions (Ley, Hamady, et al, ; Xue et al, ). The gastrointestinal tract (GIT) of carnivorous animals is relatively simple compared to those of omnivores and herbivores (Schwab & Gänzle, ; Xue et al, ). It is widely believed that herbivores have the highest microbiome diversity followed by omnivores and then carnivores (Ley, Hamady, et al, ).…”

Comparative Analysis of the Gut Microbial Communities in Forest and Alpine Musk Deer Using High-Throughput Sequencing

“…Fecal sampling is also non-invasive and is therefore beneficial for endangered or cryptic species. High-throughput sequencing of fecal DNA can elucidate bacterial communities and is attractive because it effectively deals with mixed DNA templates (Hamady et al, 2008) and several recent studies have employed these technologies to explore the microbiota of humans (Yatsunenko et al, 2012), Giant Panda (Xue et al, 2015), cattle (Shanks et al, 2011), horse (Shepherd et al, 2012), elk and white tailed deer (Gruninger et al, 2014). The colonization and diversity of gastrointestinal bacterial communities can also be affected by many biotic and abiotic factors, including host age (Claesson et al, 2011; Jami et al, 2013), host species (Shepherd et al, 2012; Gruninger et al, 2014), host stress (Bailey et al, 2010), host diseases (Andersson et al, 2008; Larsen et al, 2010), diet composition (Shanks et al, 2011), drugs exposure (Dethlefsen et al, 2008), geographical location (Linnenbrink et al, 2013; Maurice et al, 2015; Henderson et al, 2016), and environment (Sullam et al, 2012; Gruninger et al, 2014).…”

The giant panda gut microbiome

“…A recent and large study by Xue et al [9] used 16S ribosome RNA methods to uncover gut symbionts across three different seasons in 45 giant pandas born in captivity. Much variation was found in the diversity and structure of the gut microbiota across seasons and between individuals, and low gut microbial diversity dominated by Proteobacteria and Firmicutes confirmed the findings of Zhu et al [8] (Figure 1).…”