Local environment shapes milk microbiomes while evolutionary history constrains milk macronutrients in captive cercopithecine primates.

Milk is a complex biochemical fluid that includes macronutrients and microbiota, which, together, are known to facilitate infant growth, mediate the colonization of infant microbiomes, and promote immune development. Examining factors that shape milk microbiomes and milk-nutrient interplay across host taxa is critical to resolving the evolution of the milk environment. Using a comparative approach across four cercopithecine primate species housed at three facilities under similar management conditions, we test for the respective influences of the local environment (housing facility) and host species on milk (a) macronutrients (fat, sugar, and protein), (b) microbiomes (16S rRNA), and (c) predicted microbial functions. We found that milk macronutrients were structured according to host species, while milk microbiomes and predicted function were strongly shaped by the local environment and, to a lesser extent, host species. The milk microbiomes of rhesus macaques (Macaca mulatta) at two different facilities more closely resembled those of heterospecific facility-mates compared to conspecifics at a different facility. We found similar, facility-driven patterns of microbial functions linked to physiology and immune modulation, suggesting that milk microbiomes may influence infant health and development. These results provide novel insight into the complexity of milk and its potential impact on infants across species and environments.

Biodiversity of protists and nematodes in the wild nonhuman primate gut.

Documenting the natural diversity of eukaryotic organisms in the nonhuman primate (NHP) gut is important for understanding the evolution of the mammalian gut microbiome, its role in digestion, health and disease, and the consequences of anthropogenic change on primate biology and conservation. Despite the ecological significance of gut-associated eukaryotes, little is known about the factors that influence their assembly and diversity in mammals. In this study, we used an 18S rRNA gene fragment metabarcoding approach to assess the eukaryotic assemblage of 62 individuals representing 16 NHP species. We find that cercopithecoids, and especially the cercopithecines, have substantially higher alpha diversity than other NHP groups. Gut-associated protists and nematodes are widespread among NHPs, consistent with their ancient association with NHP hosts. However, we do not find a consistent signal of phylosymbiosis or host-species specificity. Rather, gut eukaryotes are only weakly structured by primate phylogeny with minimal signal from diet, in contrast to previous reports of NHP gut bacteria. The results of this study indicate that gut-associated eukaryotes offer different information than gut-associated bacteria and add to our understanding of the structure of the gut microbiome.

Convergence of human and Old World monkey gut microbiomes demonstrates the importance of human ecology over phylogeny.

BACKGROUND: Comparative data from non-human primates provide insight into the processes that shaped the evolution of the human gut microbiome and highlight microbiome traits that differentiate humans from other primates. Here, in an effort to improve our understanding of the human microbiome, we compare gut microbiome composition and functional potential in 14 populations of humans from ten nations and 18 species of wild, non-human primates. RESULTS: Contrary to expectations from host phylogenetics, we find that human gut microbiome composition and functional potential are more similar to those of cercopithecines, a subfamily of Old World monkey, particularly baboons, than to those of African apes. Additionally, our data reveal more inter-individual variation in gut microbiome functional potential within the human species than across other primate species, suggesting that the human gut microbiome may exhibit more plasticity in response to environmental variation compared to that of other primates. CONCLUSIONS: Given similarities of ancestral human habitats and dietary strategies to those of baboons, these findings suggest that convergent ecologies shaped the gut microbiomes of both humans and cercopithecines, perhaps through environmental exposure to microbes, diet, and/or associated physiological adaptations. Increased inter-individual variation in the human microbiome may be associated with human dietary diversity or the ability of humans to inhabit novel environments. Overall, these findings show that diet, ecology, and physiological adaptations are more important than host-microbe co-diversification in shaping the human microbiome, providing a key foundation for comparative analyses of the role of the microbiome in human biology and health.

Gut microbiomes of wild great apes fluctuate seasonally in response to diet.

The microbiome is essential for extraction of energy and nutrition from plant-based diets and may have facilitated primate adaptation to new dietary niches in response to rapid environmental shifts. Here we use 16S rRNA sequencing to characterize the microbiota of wild western lowland gorillas and sympatric central chimpanzees and demonstrate compositional divergence between the microbiotas of gorillas, chimpanzees, Old World monkeys, and modern humans. We show that gorilla and chimpanzee microbiomes fluctuate with seasonal rainfall patterns and frugivory. Metagenomic sequencing of gorilla microbiomes demonstrates distinctions in functional metabolic pathways, archaea, and dietary plants among enterotypes, suggesting that dietary seasonality dictates shifts in the microbiome and its capacity for microbial plant fiber digestion versus growth on mucus glycans. These data indicate that great ape microbiomes are malleable in response to dietary shifts, suggesting a role for microbiome plasticity in driving dietary flexibility, which may provide fundamental insights into the mechanisms by which diet has driven the evolution of human gut microbiomes.

Transmissible lymphoma and simian acquired immunodeficiency syndrome in rhesus monkeys.

Four rhesus monkeys (Macaca mulatta) were inoculated with a homogenate of a cutaneous lepromatous leprosy lesion from a mangabey monkey (Cercocebus atys). One died of B-cell lymphoma, and another died of an immunodeficiency syndrome. Cell suspensions prepared from the tumor and spleen of the monkey with lymphoma induced lymphoma or an immunodeficiency syndrome when inoculated into additional young rhesus monkeys. The immunodeficiency syndrome was similar to simian acquired immunodeficiency syndrome and consisted of opportunistic infections, lymphoid hyperplasia or atrophy, wasting, and syncytial cell formation. Mitogen responses and percentages of T4- and T8-positive lymphocytes were normal until the animals were moribund. Lymphoblastoid cell lines became established in vitro from tumor cell suspensions. These cells were infected with a herpesvirus related to Epstein-Barr virus. In addition, a retrovirus morphologically similar to human T-cell lymphotrophic virus type III (HTLV-III) and simian T-lymphotrophic virus type III (STLV-III) was isolated from one of the lymphoblastoid cell lines (LCL). Type D retroviruses could not be demonstrated in the monkeys in the transmission study; however, a retrovirus similar to that in the LCL was isolated from 4 animals by coculture of peripheral blood lymphocytes with the human cell line H9. These results suggest that this retrovirus, STLV-III/Delta, may be associated with the immunodeficiency syndrome in these macaques and may be of mangabey origin.

Prevalence of natural infection with simian immunodeficiency virus and simian T-cell leukemia virus type I in a breeding colony of sooty mangabey monkeys.

The seroprevalence of antibodies to simian immunodeficiency virus (SIVsmm) and simian T-cell leukemia virus type I (STLV-I) in a captive breeding colony of sooty mangabey monkeys was determined, and infection by SIVsmm was confirmed in all cases by virus isolation. Among 138 animals tested, 57 and 33% were infected with SIVsmm and STLV-I, respectively. While the proportion of female mangabeys (66%) differed significantly (P less than 0.01) from the proportion of male mangabeys (42%) infected with SIVsmm, the proportions of males and females infected with STLV-I were similar, suggesting independent transmission of the two viruses. Among mangabeys less than 1 year old, none were infected with STLV-I and only five of 27 mangabeys, all of which were at least 6 months old when first tested, were infected with SIVsmm. The data document that natural infection of sooty mangabey monkeys with SIVsmm or in association with STLV-I infection does not result in increased disease or mortality, and that transmission of both SIVsmm and STLV-I appears to occur primarily through sexual activity.

Tuberculosis in imported nonhuman primates--United States, June 1990-May 1993.

Nonhuman primates (NHPs) shipped to the United States must be quarantined and monitored for evidence of infectious diseases transmissible to humans. During May-October 1992, CDC investigated reports from NHP importers of mycobacterial infections in NHPs recently imported from Mauritius. This report describes a review of tuberculosis (TB) in all 249 imported shipments of CDC-permitted NHP species in the United States from June 1990 through May 1993 and updates recommendations regarding the identification and control of TB in imported NHPs and in workers exposed to such animals.

Experimental leprosy in African green monkeys (Cercopithecus aethiops): a model for polyneuritic leprosy.

Three African green monkeys (Cercopithecus aethiops) were inoculated intravenously and intracutaneously with Mycobacterium leprae derived from a naturally infected mangabey monkey. All developed cutaneous lesions at inoculation sites. One developed disseminated cutaneous lesions, while the cutaneous lesions in the other two regressed and eventually disappeared. The animals were examined at necropsy five years after inoculation. All three had active leprosy infection in peripheral nerves with extensive inflammation and fibrosis. The disease histologically resembled borderline-lepromatous leprosy. These findings add a new dimension to animal models of leprosy.

Homogeneity among Senegalese strains of yellow fever virus.

A series of 16 yellow fever (YF) viruses isolated from mosquitoes, monkeys and humans in different epidemiological contexts in Senegal and The Gambia between 1976 and 1983, was analyzed by T1 RNase oligonucleotide fingerprints of the genomic 32P-labeled RNA, by SDS-polyacrylamide gel electrophoresis of the intracellular virus-specified polypeptides, by peptide mapping of the envelope E glycoprotein and by immunological reactivities with monoclonal antibody fluids (MAF's) against the E glycoprotein. These strains had not been passed in suckling mice and were isolated in Aedes pseudoscutellaris Mos 61 cultured cells. These strains showed no virulence in three-week-old Swiss mice when injected intraperitoneally. Direct comparison of the large T1 RNase-resistant oligonucleotide maps indicated a relative genetic stability (92%-100%). A greater change was observed when these strains were compared with an epidemic YF strain isolated in 1965 with an oligonucleotide fingerprint map sharing 82%-88% similarity. The YF-specified proteins were identical in their molecular weight, and the fragments obtained after limited proteolysis of the envelope protein using protease V8 or alphachymotrypsine indicated that the strains were chemically similar. Only a few differences were observed when the strains were seroneutralized with MAF's, but no relation could be made with genetic or biological data. This suggested that the YF virus strains isolated from the same geographic area and during a short period of time had evolved slowly. Moreover, all the viruses were closely related and no correlation could be established with the apparent variations in virulence in nature.

Calicivirus isolation from three species of primates: an incidental finding.

Calicivirus isolations were made from 3 species of subhuman primates. Viruses were recovered from gingival lesions associated with periodontal disease in a spider monkey, from the oropharynx of a healthy silver leaf langur, and from the spleen of a lowland gorilla that had died of systemic coccidioidomycosis. Based on the results of cross-neutralization tests, all 3 isolates were serologically indistinguishable from a primate calicivirus Pan paniscus type 1. These isolations appeared to be incidental in nature and could not be associated causally with any specific disease entity.

Concurrent infection of a Patas monkey (Erythrocebus patas) by Citrobacter freundii and Trichuris trichiura.

Concurrent infection of Citrobacter freundii and Trichuris trichiura in a Patas monkey (Erythrocebus patas) is reported. A synergistic effect of both organisms contributing to host mortality in this case is suggested.

Mycobacterium bovis isolated from a dusky langur with granulomas in the intestine.

Tubercles were seen in the spleen of a male dusky langur (Presbytis obscurus) on laparotomy. Subsequently, tuberculous lesions in the intestine, lungs, and a hilar lymph node were observed on necropsy of the monkey. Histologic examinations of these tissues revealed granulomas, and acid-fast bacilli were observed within granulomas in replicate sections that were stained with auramine-O. An acid-fast organism was isolated and identified as Mycobacterium bovis. Guinea pigs and rabbits inoculated intraperitoneally with the organism developed granulomas in the lungs, liver, and spleen. Lesions did not develop in chickens inoculated with the culture.

Fatal herpesvirus infection in patas monkeys and a black and white colobus monkey.

Fatal herpesvirus infections were diagnosed in 3 patas monkeys and 1 black and white colobus monkey over a 4-week period. Herpesvirus was isolated from 1 patas monkey and from the black and white colobus monkey. Both isolates had growth characteristics similar to Herpesvirus hominis and Herpesvirus simiae. The isolate from the colobus monkey antigenically appeared to be H simiae or H simiae-like, whereas the isolate from the patas monkey could not be conclusively identified with the antisera used. All affected animals were housed in close proximity to rhesus monkeys, the carrier host of H simiae.

Serological and structural comparison of immunodeficiency viruses from man, African green monkey, rhesus monkey and sooty mangabey.

We have studied the serological relationship among the human immunodeficiency virus type 1 (HIV-1), and three simian immunodeficiency viruses (SIV). SIVagm was isolated from African green monkeys (Cercopithecus aethiops), and compared with the previously described isolates of SIVmac from a rhesus macaque (Macaca mulatta) and SIVsm from a sooty mangabey (Cercocebus atys). With respect to the glycoproteins, the simian viruses represent a subgroup apparently different from HIV. To classify HIV and SIV isolates further, we compared tryptic peptide maps of the core polypeptides p 18 and p 24 of HIV-2, three HIV-1 and five SIV isolates. Each peptide map was distinguishable, and differences are most prominent between the HIV-1 group and the SIVmac/SIVsm group. HIV-2 is very similar to SIVmac and SIVsm. The three SIVagm isolates form a more heterogeneous group. The p24s of all SIVagms are more similar to the p24s of HIV-1, but with respect to p 18, one isolate is similar to HIV-1, while the two others are more related to SIVmac, SIVsm, and HIV-2.

[Morphology of coronaviruses from different species of monkeys in the Sukhumi nursery]. / Morfologiia koronavirusov raznykh vidov obez'ian Sukhumskogo pitomnika.

The ultrastructure of coronaviruses from 46 out of 111 monkeys examined (baboons, macaques, green monkeys, langurs) was studied by negative staining in homogenates of different parts of the intestinal tract, pancreatic gland, liver, kidneys, lungs, heart, and brain. Because of marked pleomorphism of coronaviruses it is suggested that morphological variants of the viruses may be distinguished. No relationship between pleomorphism of virus particles and species differences of monkeys and their organ pathology was established. Morphological signs distinguishing simian coronaviruses from those of man were noted.