David Modry

Gut Microbiome of Coexisting BaAka Pygmies and Bantu Reflects Gradients of Traditional Subsistence Patterns

To understand how the gut microbiome is impacted by human adaptation to varying environments, we explored gut bacterial communities in the BaAka rainforest hunter-gatherers and their agriculturalist Bantu neighbors in the Central African Republic. Although the microbiome of both groups is compositionally similar, hunter-gatherers harbor increased abundance of Prevotellaceae, Treponema, and Clostridiaceae, while the Bantu gut microbiome is dominated by Firmicutes. Comparisons with US Americans reveal microbiome differences between Africans and westerners but show western-like features in the Bantu, including an increased abundance of predictive carbohydrate and xenobiotic metabolic pathways. In contrast, the hunter-gatherer gut shows increased abundance of predicted virulence, amino acid, and vitamin metabolism functions, as well as dominance of lipid and amino-acid-derived metabolites, as determined through metabolomics. Our results demonstrate gradients of traditional subsistence patterns in two neighboring African groups and highlight the adaptability of the microbiome in response to host ecology.

Gut microbiome composition and metabolomic profiles of wild western lowland gorillas (Gorilla gorilla gorilla) reflect host ecology

The metabolic activities of gut microbes significantly influence host physiology; thus, characterizing the forces that modulate this micro‐ecosystem is key to understanding mammalian biology and fitness. To investigate the gut microbiome of wild primates and determine how these microbial communities respond to the hosts external environment, we characterized faecal bacterial communities and, for the first time, gut metabolomes of four wild lowland gorilla groups in the Dzanga‐Sangha Protected Areas, Central African Republic. Results show that geographical range may be an important modulator of the gut microbiomes and metabolomes of these gorilla groups. Distinctions seemed to relate to feeding behaviour, implying energy harvest through increased fruit consumption or fermentation of highly fibrous foods. These observations were supported by differential abundance of metabolites and bacterial taxa associated with the metabolism of cellulose, phenolics, organic acids, simple sugars, lipids and sterols between gorillas occupying different geographical ranges. Additionally, the gut microbiomes of a gorilla group under increased anthropogenic pressure could always be distinguished from that of all other groups. By characterizing the interplay between environment, behaviour, diet and symbiotic gut microbes, we present an alternative perspective on primate ecology and on the forces that shape the gut microbiomes of wild primates from an evolutionary context.

Temporal variation selects for diet-microbe co-metabolic traits in the gut of Gorilla spp.

Although the critical role that our gastrointestinal microbes play in host physiology is now well established, we know little about the factors that influenced the evolution of primate gut microbiomes. To further understand current gut microbiome configurations and diet–microbe co-metabolic fingerprints in primates, from an evolutionary perspective, we characterized fecal bacterial communities and metabolomic profiles in 228 fecal samples of lowland and mountain gorillas (G. g. gorilla and G. b. beringei, respectively), our closest evolutionary relatives after chimpanzees. Our results demonstrate that the gut microbiomes and metabolomes of these two species exhibit significantly different patterns. This is supported by increased abundance of metabolites and bacterial taxa associated with fiber metabolism in mountain gorillas, and enrichment of markers associated with simple sugar, lipid and sterol turnover in the lowland species. However, longitudinal sampling shows that both species’ microbiomes and metabolomes converge when hosts face similar dietary constraints, associated with low fruit availability in their habitats. By showing differences and convergence of diet–microbe co-metabolic fingerprints in two geographically isolated primate species, under specific dietary stimuli, we suggest that dietary constraints triggered during their adaptive radiation were potential factors behind the species-specific microbiome patterns observed in primates today.

Phylogeny and sequence variability of the Sarcocystis singaporensis Zaman and Colley, (1975) 1976 ssrDNA

Abstract. The coccidium Sarcocystis singaporensis (Apicomplexa: Sarcocystidae) is a cyst-forming parasite with potential as a biological agent for the control of wild populations of rodents in non-native environments. Phylogenetic analysis based on the ssrDNA supports S. singaporensis isolates as a sister species to sarcosporidians transmitted between snakes and rodents but an association with the carnivore-ruminant Sarcocystis spp. could not be rejected by likelihood ratio tests. Four complete and six partial ssrDNA sequences representing this species are monophyletic in any tree reconstruction method; however, they possess very high pairwise distances of up to 0.053. The obtained sequences suggest the probable existence of at least two divergent paralogous ssrDNAs. Moreover, our results support the co-evolution of lsrDNA and ssrDNA in S. singaporensis. The utility of coccidian lsrDNA and ssrDNA for evolutionary studies and their abundance in the primary nucleotide databases is discussed.

Strongyloides infections of humans and great apes in Dzanga-Sangha Protected Areas, Central African Republic and in degraded forest fragments in Bulindi, Uganda.

DNA sequence analysis was carried out on Strongyloides spp. larvae obtained from fecal samples of local humans, a wild western lowland gorilla (Gorilla gorilla gorilla) and a central chimpanzee (Pan troglodytes troglodytes) inhabiting Dzanga-Sangha Protected Areas (DSPA), Central African Republic, and eastern chimpanzees (Pan troglodytes schweinfurthii) living in degraded forest fragments on farmland in Bulindi, Uganda. From humans, both Strongyloides fuelleborni and Strongyloides stercoralis were recorded, though the former was predominant. Only S. fuelleborni was present in the great apes in both areas. Phylogenetic analysis of partial mtDNA cytochrome c oxidase subunit 1 gene (Cox1) and comparison of 18S rDNA hyper variable region IV (HVR-IV) sequences implied that in DSPA S. fuelleborni populations in humans differ from those in the nonhuman great apes.

Genetic diversity of the class II major histocompatibility DRA locus in European, Asiatic and African domestic donkeys.

The major histocompatibility complex (MHC) genes coding for antigen presenting molecules are the most polymorphic genes in vertebrate genome. The MHC class II DRA gene shows only small variation in many mammalian species, but it exhibits relatively high level of polymorphism in Equidae, especially in donkeys. This extraordinary degree of polymorphism together with signatures of selection in specific amino acids sites makes the donkey DRA gene a suitable model for population diversity studies. The objective of this study was to investigate the DRA gene diversity in three different populations of donkeys under infectious pressure of protozoan parasites, Theileria equi and Babesia caballi. Three populations of domestic donkeys from Italy (N = 68), Jordan (N = 43), and Kenya (N = 78) were studied. A method of the donkey MHC DRA genotyping based on PCR-RFLP and sequencing was designed. In addition to the DRA gene, 12 polymorphic microsatellite loci were genotyped. The presence of Theileria equi and Babesia caballi parasites in peripheral blood was investigated by PCR. Allele and genotype frequencies, observed and expected heterozygosities and F(IS) values were computed as parameters of genetic diversity for all loci genotyped. Genetic distances between the three populations were estimated based on F(ST) values. Statistical associations between parasite infection and genetic polymorphisms were sought. Extensive DRA locus variation characteristic for Equids was found. The results showed differences between populations both in terms of numbers of alleles and their frequencies as well as variation in expected heterozygosity values. Based on comparisons with neutral microsatellite loci, population sub-structure characteristics and association analysis, convincing evidence of pathogen-driven selection at the population level was not provided. It seems that genetic diversity observed in the three populations reflects mostly effects of selective breeding and their different genetic origins.

How many species of whipworms do we share? Whipworms from man and other primates form two phylogenetic lineages.

Abstract: The whipworms, i.e. parasitic nematodes of the genus Trichuris Roederer, 1761, infect a variety of mammals. Apparently low diversity of primate-infecting species of Trichuris strongly contrasts with the high number of species described in other mammalian hosts. The present study addresses the diversity of whipworms in captive and free-ranging primates and humans by analysing nuclear (18S rRNA, ITS2) and mitochondrial (cox1) DNA. Phylogenetic analyses revealed that primate whipworms form two independent lineages: (i) the Trichuris trichiura (Linnaeus, 1771) clade comprised of genetically almost identical whipworms from human and other primates, which suggests the ability of T. trichiura to infect a broader range of primates; (ii) a clade containing primarily Trichuris suis Schrank, 1788, where isolates from human and various primates formed a sister group to isolates from pigs; the former isolates thus may represent of more species of Trichuris in primates including humans. The analysis of cox1 has shown the polyphyly of the genera Trichuris and Capillaria, Zeder, 1800. High sequence similarity of the T. trichiura isolates from humans and other primates suggests their zoonotic potential, although the extent of transmission between human and other non-human primates remains questionable and requires further study.

Erratum: Temporal variation selects for diet-microbe co-metabolic traits in the gut of Gorilla spp (The ISME Journal (2016) 10, 532; (DOI:10.1038/ismej.2015.252))

After the publication of this paper, the author noticed an error in the affiliations concerning Klara Petrzelkova and David Modry. The affiliations are as follows: For Klara Petrzelkova, it is the Institute of Vertebrate Biology, Academy of Sciences of the Czech Republic, Brno, Czech Republic; Biology Centre, Institute of Parasitology, Academy of Sciences of the Czech Republic, Ceske Budejovice, Czech Republic; and Liberec Zoo, Liberec, Czech Republic. For David Modry, it is the Department of Pathology and Parasitology, Faculty of Veterinary Medicine, University of Veterinary and Pharmaceutical Sciences Brno, Czech Republic; Biology Centre, Institute of Parasitology, Academy of Sciences of the Czech Republic, Ceske Budejovice, Czech Republic; and CEITEC, Central European Institute for Technology, Brno, Czech Republic. The authors would like to apologise for any inconvenience this may have caused. The ISME Journal (2016) 10, 532

MYD88 and functionally related genes are associated with multiple infections in a model population of Kenyan village dogs

The purpose of this study was to seek associations between immunity-related molecular markers and endemic infections in a model population of African village dogs from Northern Kenya with no veterinary care and no selective breeding. A population of village dogs from Northern Kenya composed of three sub-populations from three different areas (84, 50 and 55 dogs) was studied. Canine distemper virus (CDV), Hepatozoon canis, Microfilariae (Acantocheilonema dracunculoides, Acantocheilonema reconditum) and Neospora caninum were the pathogens studied. The presence of antibodies (CDV, Neospora), light microscopy (Hepatozoon) and diagnostic PCR (Microfilariae) were the methods used for diagnosing infection. Genes involved in innate immune mechanisms, NOS3, IL6, TLR1, TLR2, TLR4, TLR7, TLR9, LY96, MYD88, and three major histocompatibility genes class II genes were selected as candidates. Single nucleotide polymorphism (SNP) markers were detected by Sanger sequencing, next generation sequencing and PCR-RFLP. The Fisher´s exact test for additive and non-additive models was used for association analyses. Three SNPs within the MYD88 gene and one TLR4 SNP marker were associated with more than one infection. Combined genotypes and further markers identified by next generation sequencing confirmed associations observed for individual genes. The genes associated with infection and their combinations in specific genotypes match well our knowledge on their biological role and on the role of the relevant biological pathways, respectively. Associations with multiple infections observed between the MYD88 and TLR4 genes suggest their involvement in the mechanisms of anti-infectious defenses in dogs.

Ecological and evolutionary adaptations shape the gut microbiome of BaAka African rainforest hunter-gatherers

The gut microbiome provides access to otherwise unavailable metabolic and immune functions, likely affecting mammalian fitness and evolution. To investigate how this microbial ecosystem impacts evolutionary adaptation of humans to particular habitats, we explore the gut microbiome and metabolome of the BaAka rainforest hunter-gatherers from Central Africa. The data demonstrate that the BaAka harbor a colonic ecosystem dominated by Prevotellaceae and other taxa likely related to an increased capacity to metabolize plant structural polysaccharides, phenolics, and lipids. A comparative analysis shows that the BaAka gut microbiome shares similar patterns with that of the Hadza, another hunter-gatherer population from Tanzania. Nevertheless, the BaAka harbor significantly higher bacterial diversity and pathogen load compared to the Hadza, as well as other Western populations. We show that the traits unique to the BaAka microbiome and metabolome likely reflect adaptations to hunter-gatherer lifestyles and particular subsistence patterns. We hypothesize that the observed increase in microbial diversity and potential pathogenicity in the BaAka microbiome has been facilitated by evolutionary adaptations in immunity genes, resulting in a more tolerant immune system. Significance Human ecological adaptation requires changes at the genomic level. However, the gut microbiome, the collection of microbes inhabiting the gastrointestinal tract and their functions, also responds significantly to ecological challenge. To determine how the gut microbiome responds to evolutionary adaptations in the host, we profiled gut bacterial communities of the BaAka, rainforest hunter-gatherers from Central Africa. The gut microbiome of the BaAka shows adaptations to metabolize foods rich in fiber, tannins and fats. Similarly, higher bacterial diversity and abundance of pathogenic bacteria, compared to other hunter-gatherers and western populations, suggest that the BaAka immune system evolved to coexist with increased pathogen threats. Accordingly, these results show how the gut microbiome contributes to human ecological plasticity, impacting host adaptation and evolution.