Habitat degradation impacts black howler monkey (Alouatta pigra) gastrointestinal microbiomes

Abstract

The gastrointestinal (GI) microbiome contributes significantly to host nutrition and health. However, relationships involving GI microbes, their hosts and host macrohabitats remain to be established. Here, we define clear patterns of variation in the GI microbiomes of six groups of Mexican black howler monkeys (Alouatta pigra) occupying a gradation of habitats including a continuous evergreen rainforest, an evergreen rainforest fragment, a continuous semi-deciduous forest and captivity. High throughput microbial 16S ribosomal RNA gene sequencing indicated that diversity, richness and composition of howler GI microbiomes varied with host habitat in relation to diet. Howlers occupying suboptimal habitats consumed less diverse diets and correspondingly had less diverse gut microbiomes. Quantitative real-time PCR also revealed a reduction in the number of genes related to butyrate production and hydrogen metabolism in the microbiomes of howlers occupying suboptimal habitats, which may impact host health.

Figure 1

Howler microbiomes clustered by host habitat. (a) Rarefaction curves show the number of unique Operational taxonomic units (sharing⩾97% sequence identity) per total reads for each sample. Analysis of variance of the log-linear regression coefficients for each curve confirmed habitat differences (F_{3, 31}=28.91, P<0.0001). (b) Dendrogram compares sample pairs using Bray-Curtis similarity indices. Individual identities and groups are listed in Table 1. ANOSIM tests habitat clustering using permutations (ANOSIM R=0.743, P=0.001). The CR outlier is the same individual in both panels.

Figure 2

(a) Abundance (±s.d.) of metabolic functional genes in the microbiomes of howlers across habitats as determined by qRT–PCR. Genes targeted included acs for acetogens, mcrA for methanogens, dsrA for sulfate reducers, (NF)hyd for hydrogen producers, and BcoA for butyrate producers. (b) Prevalence of the butyryl-CoA:acetate CoA-transferase gene for butyrate producers across habitats. Letters indicate significantly different abundances among habitats (t-tests, P<0.05). Prevalence of all genes except those involved in butyrate production was 100% for all habitats. Patterns are similar when groups are taken into account within habitats.