Interactions between Human Gut Microbiome Dynamics and Sub-Optimal Health Symptoms during Seafaring Expeditions

During long ocean voyages, crew members are subject to complex pressures from their living and working environment, which lead to chronic diseases-like sub-optimal health status. Although the association between dysbiotic gut microbiome and chronic diseases has been broadly reported, the correlation between the sub-optimal health status and gut microbiome remains elusive. Here, the health status of 77 crew members (20-35 years old Chinese, male) during a 135-day sea expedition was evaluated using the shotgun metagenomics of stool samples and health questionnaires taken before and after the voyage. We found five core symptoms (e.g., abnormal defecation frequency, insomnia, poor sleep quality, nausea, and overeating) in 55 out of 77 crew members suffering from sub-optimal health status, and this was termed "seafaring syndrome" (SS) in this study. Significant correlation was found between the gut microbiome and SS rather than any single symptom. For example, SS was proven to be associated with individual perturbation in the gut microbiome, and the microbial dynamics between SS and non-SS samples were different during the voyage. Moreover, the microbial signature for SS was identified using the variation of 19 bacterial species and 26 gene families. Furthermore, using a Random Forest model, SS was predicted with high accuracy (84.4%, area under the concentration-time curve = 0.91) based on 28 biomarkers from pre-voyage samples, and the prediction model was further validated by another 30-day voyage cohort (accuracy = 83.3%). The findings in this study provide insights to help us discover potential predictors or even therapeutic targets for dysbiosis-related diseases. IMPORTANCE Systemic and chronic diseases are important health problems today and have been proven to be strongly associated with dysbiotic gut microbiome. Studying the association between the gut microbiome and sub-optimal health status of humans in extreme environments (such as ocean voyages) will give us a better understanding of the interactions between observable health signs and a stable versus dysbiotic gut microbiome states. In this paper, we illustrated that ocean voyages could trigger different symptoms for different crew member cohorts due to individual differences; however, the co-occurrence of high prevalence symptoms indicated widespread perturbation of the gut microbiome. By investigating the microbial signature and gut microbiome dynamics, we demonstrated that such sub-optimal health status can be predicted even before the voyage. We termed this phenomenon as "seafaring syndrome." This study not only provides the potential strategy for health management in extreme environments but also can assist the prediction of other dysbiosis-related diseases.