Père David's deer gut microbiome changes across captive and translocated populations: Implications for conservation

Abstract

The gut microbial composition and function are shaped by different factors (e.g., host diet and phylogeny). Gut microbes play an important role in host nutrition and development. The gut microbiome may be used to evaluate the host potential environmental adaptation. In this study, we focused on the coevolution of the gut microbiome of captive and translocated Père David's deer populations (Elaphurus davidianus; Chinese: Père David's deer). To address this, we used several different macro- and micro-ecological approaches (landscape ecology, nutritional methods, microscopy, isotopic analysis, and metagenomics). In this long-term study (2011-2014), we observed some dissimilarities in gut microbiome community and function between the captive and wild/translocated Dafeng Père David's deer populations. These differences might link microbiome composition with deer diet within a given season. The proportion of genes coding for putative enzymes (endoglucanase, beta-glucosidase, and cellulose 1,4-beta-cellobiosidase) involved in cellulose digestion in the gut microbiome of the captive populations was higher than that of the translocated population, possibly because of the high proportion of cellulose, hemicellulose, and lignin in the plants most consumed by the captive populations. However, the two enzymes (natA and natB) involved in sodium transport system were enriched in the gut microbiome in translocated population, possibly because of their high salt diet (e.g., Spartina alterniflora). Thus, our results suggested that Père David's deer gut microorganisms potentially coevolved with host diet, and reflected the local adaptation of translocated population in the new environment (e.g., new dietary plants: Spartina alterniflora). A current problem for Père David's deer conservation is the saturation of captive populations. Given that the putative evolutionary adaptation of Père David's deer gut microbiome and its possible applications in conservation, the large area of wetlands along the Yellow Sea dominated by S. alterniflora might be the major translocation region in the future.

Keywords: Père David’s deer; coevolution; conservation; gut microbiome; sodium transport system; translocated populations.

Figure 1

The study area. (a) The main Père David's deer populations in China: Dafeng Natural Reserve (DF), Jiangsu; Hubei Shishou Natural Reserve (HB), Hubei; and Beijing Nanhaizi Natural Reserve (BJ), Beijing. (b) The satellite map of DF (composed of three core areas: DFI, DFII, and DFIII), which holds the largest Père David's deer population in the world. (c) The wild habitat (DFIII) in 2013. Shown is the distribution of plants, including Spartina (SAL: Spartina alterniflora.), Imperate (ICY: Imperata cylindrica var. major), Salsa (SGL: Suaeda glauca), Reed (PAU: Phragmites australis), sea water, and roads. (d) The distribution range of SAL (purple regions in Jiangsu and Shanghai provinces were sketched using the record from our previous surveys)

Figure 2

The stable carbon and nitrogen isotopes in Père David's deer habitats. (a) Isotopic changes in (b) DFI and DFII, and (c) DFIII. (d) Isotopic changes in the summer. (e) Isotopic changes in the winter. (f) The nutritional composition of the main eating plants in DFI‐II and DFIII

Figure 3

Gut microbial community dynamics in Père David's deer populations. (a) The dominant phyla. (b) The dominant families

Figure 4

The PoCA analysis of captive and translocated populations. (a) Summer sampling season. (b) Winter sampling season. (c–d) Random forest tests for (c) the summer sampling season and (d) the winter sampling season

Figure 5

The potential adaptation on high‐salt diet by gut microbial from Père David's deer metagenomes. (a, b) The proportion of genes coding for these putative enzymes (natA and natB) related to the potential sodium transport system in Père David's deer gut microbiomes. The taxonomic assignment of the identified genes coding for natA (c) and natB (d)

Figure 6

The potential for cellulose degradation by gut microbial from Père David's deer metagenomes. (a) The proportion of genes coding for these putative vital enzymes (endoglucanase, beta‐glucosidase, and cellulose 1,4‐beta‐cellobiosidase) related to the potential cellulose digestion in Père David's deer gut microbiomes. The taxonomic assignment of the identified genes coding for endoglucanase (b), beta‐glucosidase (c), and cellulose 1,4‐beta‐cellobiosidase (d)

Figure 7

The relative abundance (16S) of some genera related to potential cellulose and sodium metabolisms in Père David's deer's feces among three populations (two captive populations: DFI and DFII, one translocated population: DFIII). (a) Linear discriminant analysis (LDA) effect size (LEfSe) method identified significant variations in the compositional profile (16S) at genus level among these populations (threshold on the logarithmic LDA score: 2.5). The relative abundance of Ruminococcus (b), Methanocorpusculum (c), and Bacteroides (d)