Fecal bacterial communities of wild black capuchin monkeys (Sapajus nigritus) from the Atlantic Forest biome in Southern Brazil are divergent from those of other non-human primates

Tiela Trapp Grassotti; Caroline Isabel Kothe; Janira Prichula; Nacer Mohellibi; Michele Bertoni Mann; Paulo Guilherme Carniel Wagner; Fabricio Souza Campos; Aline Alves Scarpellini Campos; Jeverson Frazzon; Ana Paula Guedes Frazzon

doi:10.1016/j.crmicr.2021.100048

Fecal bacterial communities of wild black capuchin monkeys (Sapajus nigritus) from the Atlantic Forest biome in Southern Brazil are divergent from those of other non-human primates

Curr Res Microb Sci. 2021 Jul 10:2:100048. doi: 10.1016/j.crmicr.2021.100048. eCollection 2021 Dec.

Affiliations

¹ Post-Graduation Program in Agricultural and Environmental Microbiology, Microbiology, Immunology, and Parasitology Department, Institute of Basic Health Sciences, Federal University of Rio Grande do Sul, Porto Alegre, RS, Brazil.
² Université Paris-Saclay, INRAE, AgroParisTech, Micalis Institute, Jouy-en-Josas, France.
³ Department of Health Sciences, Federal University of Health Sciences of Porto Alegre, Porto Alegre, RS, Brazil.
⁴ Brazilian Institute of Environment and Renewable Natural Resources, IBAMA, Brasília, Brazil.
⁵ Laboratory of Bioinformatics and Biotechnology, Campus de Gurupi, Federal University of Tocantins, Gurupi, TO, Brazil; Federal University of Tocantins, Federal University of Tocantins, Palmas, TO, Brazil.
⁶ State Center for Health Surveillance, State Secretariat for Health of Rio Grande do Sul, Porto Alegre, RS, Brazil.
⁷ Biochemistry and Molecular Biology of Microorganisms Laboratory, Institute of Food Science and Technology, Federal University of Rio Grande do Sul, Porto Alegre, RS, Brazil.

Abstract

Gut microbiota are influenced by factors such as diet, habitat, and social contact, which directly affect the host's health. Studies related to gut microbiota in non-human primates are increasing worldwide. However, little remains known about the gut bacterial composition in wild Brazilian monkeys. Therefore, we studied the fecal microbiota composition of wild black capuchin monkey (Sapajus nigritus) (n=10) populations from two different Atlantic Forest biome fragments (five individuals per fragment) in south Brazil. The bacterial community was identified via the high-throughput sequencing and partial amplification of the 16S rRNA gene (V4 region) using an Ion Personal Genome Machine (PGM^TM) System. In contrast to other studies involving monkey microbiota, which have generally reported the phyla Firmicutes and Bacteroidetes as predominant, black capuchin monkeys showed a high relative abundance of Proteobacteria ( $\bar{χ}$ = 80.54%), followed by Firmicutes ( $\bar{χ}$ = 12.14%), Actinobacteria ( $\bar{χ}$ = 4.60%), and Bacteriodetes ( $\bar{χ}$ = 1.31%). This observed particularity may have been influenced by anthropogenic actions related to the wild habitat and/or diet specific to the Brazilian biome's characteristics and/or monkey foraging behavior. Comparisons of species richness (Chao1) and diversity indices (Simpson and InvSimpson) showed no significant differences between the two groups of monkeys. Interestingly, PICRUSt2 analysis revealed that metabolic pathways present in the bacterial communities were associated with xenobiotic biodegradation and the biosynthesis of secondary metabolites, which may suggest positive effects on monkey health and conservation in this anthropogenic habitat. Infectious disease-associated microorganisms were also observed in the samples. The present study provides information about the bacterial population and metabolic functions present in fecal microbiota, which may contribute to a better understanding of the ecology and biology of black capuchin monkeys living in forest fragments within the Atlantic Forest biome in southern Brazil. Additionally, the present study demonstrates that the fecal bacterial communities of wild black capuchin monkeys in this area are divergent from those of other wild non-human primates.

Keywords: FROGS, Find Rapidly OTUs with Galaxy Solution; FastQC, Fast Quality Control; Fecal microbiota; HTS, high-throughput sequencing; KEGG, Kyoto Encyclopedia of Genes and Genomes; MultiQC, Multi Quality Control; OTUs, Operational Taxonomic Units; PGMTM, Personal Genome Machine; PICRUSt2, Phylogenetic Investigation of Communities by Reconstruction of Unobserved State; Primate conservation; Proteobacteria; Robust capuchins; SCS, Santa Cruz do Sul; SSC, São Sebastião do Caí; SSU, Small Subunit rRNA gene; Wild south Brazilian primates.