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

ABSTRACT 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.

. Annotation for microbial species in the co-occurrence network 6   Table S2. The important score of the 28 microbial species and functions used in the 7 Random Forest model 8   Table S3. Definitions of the 24 indicators in the questionnaire 9   Table S4. The questionnaire answers for all individuals before and after the voyage

Body mass index (BMI)
The BMI is defined as the body mass divided by the square of the body height (1).

Backache
Back pain, also known as backache, is pain felt in the back (2).

Headache
It is usually confined to the upper part of the head, including the upper edge of the eyebrow arch, the helix and the pain above the line connecting the external occipital protuberance (3).

Stomachache
Stomach pain refers to the pain in the epigastric part of the upper abdomen, above the connection line between the lower edges of ribs on both sides and near the heart socket under the xiphoid process (4).

Muscular soreness
Pain or tenderness in one or more muscles which can involve any area of the body.

Dyspnea
Dyspnea is a combination of subjective feeling and objective signs. Subjectively, breathing is laborious, objectively, the number of breaths increases, the movement is fast and the range increases (6).

Palpitation
Palpitation includes palpitation and palpitation, which is a kind of uncomfortable feeling or palpitation of conscious heart beating (7).

Insomnia
Insomnia is medically defined as being unable to fall asleep or remain asleep, resulting in insufficient sleep (8).
Shallow sleep Difficulty in falling asleep, decreased sleep quality and sleep time.
Over-eating Overeating means taking a huge amount of food in a very short time (9).

Nausea
Nausea is a kind of gastric discomfort that can cause vomiting impulse (10).

Inactivity
People's mental and physical abilities are not as good as before, and will feel tired when they engage in daily activities (11).
Poor appetite Lack of appetite or lack the desire to eat (12).

Feelings of loneliness
Loneliness is an unpleasant emotional response to perceived isolation (13).
Depression Depression (mood), a state of low mood and aversion to activity (14).
Self-accusation Self-accusation is a cognitive process in which an individual attributes the occurrence of a stressful event to oneself (15).

Mistrustfulness
Mistrustfulness is an individual's distrust of other people's words, promises and statements (16).
Stool type Type 1: Separate hard lumps (like nuts), or sausage-shaped (but lumpy); Type 2: Like a sausage but with cracks on its surface (can be black);Type 3: Like a sausage or snake, smooth and soft (average stool) Type 4: Soft blobs with clear cut edges; Type 5: A mushy stool or watery (diarrhoea) (17).

Bloody stools
The color of the stool is bright red, dark red or tar like (black stool) (18).

Incomplete defecation
This term is a feeling of incomplete defecation. When defecating, even if the intestinal contents have been emptied, they still want to be discharged.

Bowel difficulties
The defecation was laborious, painful and prolonged.
Bowel movement Want to defecate but can't row out, or squat down for a long time to row out (19).
Defecation frequency (weekly) Frequency of defecation per week. The normal frequency of bowel movements in adults is between three per day and three per week (20).