Dynamics of Gut Microbiome in Giant Panda Cubs Reveal Transitional Microbes and Pathways in Early Life

Abstract

Adult giant pandas (Ailuropoda melanoleuca) express transitional characteristics in that they consume bamboos, despite their carnivore-like digestive tracts. Their genome contains no cellulolytic enzymes; therefore, understanding the development of the giant panda gut microbiome, especially in early life, is important for decoding the rules underlying gut microbial formation, inheritance and dietary transitions. With deep metagenomic sequencing, we investigated the gut microbiomes of two newborn giant panda brothers and their parents living in Macao, China, from 2016 to 2017. Both giant panda cubs exhibited progressive increases in gut microbial richness during growth, particularly from the 6th month after birth. Enterobacteriaceae dominated the gut microbial compositions in both adult giant pandas and cubs. A total of 583 co-abundance genes (CAGs) and about 79 metagenomic species (MGS) from bacteria or viruses displayed significant changes with age. Seven genera (Shewanella, Oblitimonas, Helicobacter, Haemophilus, Aeromonas, Listeria, and Fusobacterium) showed great importance with respect to gut microbial structural determination in the nursing stage of giant panda cubs. Furthermore, 10 orthologous gene functions and 44 pathways showed significant changes with age. Of the significant pathways, 16 from Escherichia, Klebsiella, Propionibacterium, Lactobacillus, and Lactococcus displayed marked differences between parents and their cubs at birth, while 29 pathways from Escherichia, Campylobacter and Lactobacillus exhibited significant increase in cubs from 6 to 9 months of age. In addition, oxidoreductases, transferases, and hydrolases dominated the significantly changed gut microbial enzymes during the growth of giant panda cubs, while few of them were involved in cellulose degradation. The findings indicated diet-stimulated gut microbiome transitions and the important role of Enterobacteriaceae in the guts of giant panda in early life.

Succession of Gut Microbial Structure in Twin Giant Pandas During the Dietary Change Stage and Its Role in Polysaccharide Metabolism

“…Enterobacter, Escherichia-Shigella, and Lactobacillus were the dominant bacterial genera in early life (Zhang et al, 2018). These populations prefer to colonize carnivore intestines and subsist on oligosaccharides, fats, amino acids, and their derivatives in cubs' food (Varrone et al, 2013;Kong et al, 2018;Li et al, 2019), and are associated with many important energy metabolism pathways (Guo M. et al, 2018); in particular, Lactobacillus is a probiotic genus in early growth of mammals (Williams et al, 2013). The relative proportion of Streptococcus increased in the cub guts after the age of 1 year when consuming the products of fibrous metabolism (Xue et al, 2015;Wang et al, 2016) in supplementary foods.…”

“…These findings demonstrate, to some extent, the important status of cellulose in the nutrient usage of the giant panda. The giant panda has evolved a pseudothumb for grasping bamboo and metabolic pathways to efficiently utilize the essential amino acids, fatty acids, and vitamins in bamboo (Hu et al, 2017;Guo M. et al, 2018) and has also established close interactions with specific gut microbes during its adaptation to a bamboo diet (Mckenney et al, 2017), not only for nutrient digestion but also for detoxification (Zhu et al, 2018). Zhang et al (2018) suggested that the intestinal microbes of the giant panda digest cellulose poorly and that the hemicellulose in their food is mainly utilized by giant panda cubs.…”

“…Giant panda cubs undergo a specific process of dietary change when they transition from milk to a high-polysaccharide bamboo diet in their adaptation to a specialized bamboo diet. This process is especially important to panda cubs, and during it, they are very fragile, with a low survival rate (Guo M. et al, 2018;Stewart et al, 2018). It is quite a complex period, but it is ideal for investigating the relationships between intestinal microbes and the polysaccharide metabolism of the giant panda.…”

Review: Other Helicobacter species

“…33 These findings provide unique insight into human CRC since human CRC molecular characteristics match those of canine tumors. 36 Weaning is a crucial period leading to serious intestinal dysbiosis and mortality in piglets. 34 A species rarely reported in dogs, "Helicobacter winghamensis," was isolated from fecal samples of working farm dogs.…”

“…35 Enterobacteriaceae dominated the gut microbial compositions in adult giant pandas and their cubs while Helicobacteraceae belonged to the seven genera that showed great importance with respect to gut microbial structural determination in the nursing stage of giant panda cubs. 36 Weaning is a crucial period leading to serious intestinal dysbiosis and mortality in piglets. Genera, such as Campylobacter, Veillonella, Helicobacter, and Blautia that were previously reported in intestinal dysbiosis, were significantly enriched in 7-day post-weaned piglets.…”