Vibrio spp.: a potential critical pathogen for mammals with implications beyond marine aquaculture

Abstract

Background: Species-specific or health status specific microbiome composition of cetaceans is still poorly classified due to the limited samples. Despite a partial identification of the gut microbiota of melon-headed whales (Peponocephala electra), comparative analyses across anatomical systems are lacking. This study provides the first comprehensive analysis of the microbial communities habiting nine body sites - oral cavity, esophagus, foregut, midgut, hindgut, blowhole, and skin wounds (left anterior, dorsal fin, tail) - in a stranded melon-headed whale.

Results: By 16 S rRNA gene sequencing, a decrease in microbial richness was observed from the oral cavity to the hindgut, accompanied by compositional shifts from Fusobacterium-dominated oral/esophageal niches to Vibrio-enriched gastrointestinal regions (21.81% Vibrio, 21.19% Fusobacterium, 12.50% Actinobacillus). The respiratory tract microbiota underwent a significant shift and was dominated by Ostreibacterium (57.5%), Helcococcus (6.59%), and Tenacibaculum (4.12%). Skin wounds showed environmental similarities, with Vibrio (47.84%), Pseudoalteromonas (17.84%), and Psychrobacter (12.36%). Pan-microbiome screening identified seven Vibrio species (V. alginolyticus, V. cidicii, V. cyclitrophicus, V. navarrensis, V. parahaemolyticus, V. salilacus, and V. splendidus) across all niches, along with V. cholerae in non-respiratory samples. Notably, V. profundi was exclusively localized to anterior and dorsal fin wounds. Functional profiling revealed enrichment of Vibrio-linked pathogenesis pathways (infection, pathogenic cycle) and metabolic modules that were correlated with immunocompromised states.

Conclusions: This study revealed significant bidirectional environment-host microbiome exchange dynamics across cetacean mucosal surfaces. Notably, Vibrio spp. emerged as the dominant genus in both gastrointestinal and cutaneous wound microbiomes, highlighting: (1) potential zoonotic transmission risks from pathogenic Vibrio strains, and (2) the critical need for habitat-specific microbial surveillance to inform marine mammal conservation strategies.

Keywords: Gastrointestinal tract; Melon-headed whale; Pathogens; Respiratory tract; Wound.

Fig. 1

Location and image of the stranded melon-headed whale

Fig. 2

Alpha diversity, including observed species (Sob) (A), Chao1 (B), Shannon (C) and Simpson (D) of the microbiome from the gastrointestinal tract, respiratory tract, wound, and water of a melon-headed whale

Fig. 3

Weighted Unifrac distance for microbiota from 9 body sites and water of the habitat effect. Colors denote the 10 samples, and shapes refer to four habitat groups. PCoA (A) and NMDS (B) revealed that microbiota varied with body sites and clustered by major habitats

Fig. 4

Relative abundance of the microbiome from the gastrointestinal tract, respiratory tract, wound, and water of a melon-headed whale at the phylum level (A), order level (B), and genus level (C)

Fig. 5

Heatmap of the relative of the relative abundance of the genus Vibrio and another potential pathogen from the gastrointestinal tract, respiratory tract, wound, and water of a melon-headed whale. log10(x*10^2)-transformed relative abundances, where x represents the proportion of each operational taxonomic unit (OTU)

Fig. 6

Functional profile of the microbial communities from the gastrointestinal tract, respiratory tract, wound, and water of a melon-headed whale predicted by PICRUSt2