Fecal microbiota dysbiosis in macaques and humans within a shared environment

Traditional zoonotic disease research focuses on detection of recognized pathogens and may miss opportunities to understand broader microbial transmission dynamics between humans, animals, and the environment. We studied human-macaque microbiome overlap in Kosum Phisai District, Maha Sarakham Province, Thailand, where a growing population of long-tailed macaques (Macaca fascicularis) in Kosumpee Forest Park interact with humans from an adjacent village. We surveyed workers in or near the park with elevated exposure to macaques to characterize tasks resulting in exposure to macaque feces in addition to dietary and lifestyle factors that influence gut microbiome composition. Fecal samples were collected from 12 exposed workers and 6 controls without macaque exposure, as well as 8 macaques from Kosumpee Forest Park and 4 from an isolated forest patch with minimal human contact. The V4 region of the 16S rRNA gene from fecal sample extracted DNA was amplified and sequenced using Illumina MiSeq to characterize the microbial community. A permuted betadisper test on the weighted UniFrac distances revealed significant differences in the dispersion patterns of gut microbiota from exposed and control macaques (p = 0.03). The high variance in gut microbiota composition of macaques in contact with humans has potential implications for gut microbiome stability and susceptibility to disease, described by the Anna Karenina principle (AKP). Human samples had homogenous variance in beta diversity but different spatial medians between groups (p = 0.02), indicating a shift in microbial composition that may be explained by fundamental lifestyle differences between the groups unrelated to exposure status. SourceTracker was used to estimate the percent of gut taxa in exposed humans that was contributed by macaques. While one worker showed evidence of elevated contribution, the overall trend was not significant. Task observations among workers revealed opportunities to employ protective measures or training to reduce exposure to occupational hazards. These results suggest the potential for hygiene measures to mitigate negative aspects of contact between humans and macaques in order to optimize the health of both populations.

传统人畜共患病研究多聚焦于已识别病原体的检测，往往错失探究人类、动物与环境间更广泛微生物传播动态的契机。本研究针对泰国玛哈沙拉堪府科穆披色县开展人与猕猴微生物组重叠特征的调查：该县科松披森林公园内的长尾猕猴（Macaca fascicularis）种群持续扩张，且与周边村落的人类存在高频互动。我们对公园内及周边接触猕猴风险较高的工作人员进行了调研，旨在明确除影响肠道微生物组组成的饮食与生活方式因素外，导致猕猴粪便接触的各类作业活动特征。本研究共采集粪便样本：12名存在猕猴接触史的工作人员、6名无猕猴接触史的对照个体，以及科松披森林公园的8只猕猴与4只栖息于人类接触极少的偏远林块的猕猴。采用Illumina MiSeq平台对粪便样本提取的DNA中的16S rRNA基因V4区进行扩增与测序，以解析微生物群落结构。对加权UniFrac距离执行置换betadisper检验结果显示，接触组与对照组猕猴的肠道菌群离散模式存在显著差异（p=0.03）。接触人类的猕猴肠道菌群组成具有较高变异性，这一现象符合安娜·卡列尼娜原则（Anna Karenina Principle, AKP），其或对肠道菌群稳定性及疾病易感性存在潜在影响。人类样本的β多样性方差均一，但组间空间中位数存在显著差异（p=0.02），表明菌群组成发生了偏移，该偏移或由两组间与接触状态无关的根本性生活方式差异所致。采用SourceTracker工具估算接触猕猴的人类肠道菌群中猕猴来源类群所占比例，尽管有1名工作人员的样本显示猕猴来源菌群占比升高，但整体趋势未达到统计学显著性。对工作人员的作业活动观察结果显示，可通过采取防护措施或开展培训来降低职业接触风险。本研究结果表明，卫生干预措施或可缓解人与猕猴接触带来的负面影响，从而优化两者的健康水平。