Bacterial dysbiosis and epithelial status of the California sea lion (Zalophus californianus) in the Gulf of California.

Despite the high incidence of urogenital carcinoma (UGC) in California sea lions stranded along California, no UGC has been reported in other areas of their distribution; however, cell morphologies typical of premalignant states have been found. Risk factors for UGC include high of organochlorines and infection with a gammaherpesvirus, OtHV-1, but the importance of the bacteriome for epithelial status remains unknown. We characterized the genital bacteriome of adult female California sea lions along their distribution in the Gulf of California and examined whether the diversity and abundance of the bacteriome varied spatially, whether there were detectable differences in the bacteriome between healthy and altered epithelia, and whether the bacteriome was different in California sea lions infected with OtHV-1 or papillomavirus. We detected 2270 ASVs in the genital samples, of which 35 met the criteria for inclusion in the core bacteriome. Fusobacteriia and Clostridia were present in all samples, at high abundances, and Actinobacteria, Alphaproteobacteria, and Campylobacteria were also well-represented. Alpha diversity and abundance of the California sea lion genital bacteriome varied geographically. The abundance of bacterial ASVs varied depending on the genital epithelial status and inflammation, with differences driven by classes Fusobacteriia, Clostridia, Campylobacteria and Alphaproteobacteria. Alpha diversity and abundance were lowest in samples in which OtHV-1 was detected, and highest those with papillomavirus. Our study is the first investigation of how the bacteriome is related to epithelial status in a wild marine species prone to developing cancer.

Melanin granules melanophages and a fully-melanized epidermis are common traits of odontocete and mysticete cetaceans.

BACKGROUND: The cellular mechanisms used to counteract or limit damage caused by exposure of marine vertebrates to solar ultraviolet (UV) radiation are poorly understood. Cetaceans are vulnerable because they lack protective skin appendages and are obliged to surface continuously to breathe, thus being exposed repeatedly to UV light. Although molecular mechanisms of photoprotection of cetaceans have been studied, there is limited knowledge about their epidermal structure and photoprotective effectors. OBJECTIVE: To describe and compare the epidermis of mysticete and odontocete cetaceans and identify potentially photoprotective traits. ANIMALS: Twenty eight free-living individuals belonging to six cetacean species were sampled in the Mexican Central Pacific and Gulf of California. Species sampled were the bottlenose dolphin, pantropical spotted dolphin, spinner dolphin, Bryde's whale, fin whale and humpback whale. METHODS: Histological and cytological evaluation of skin biopsy tissue collected in the field between 2014 and 2016. RESULTS: All cetaceans had only three epidermal layers, lacking both the stratum granulosum and stratum lucidum. A relatively thick stratum corneum with a parakeratosis-like morphology was noted. Melanin was observed within keratinocytes in all epidermal layers, including the stratum corneum and apical melanin granules obscured the keratinocyte nucleus. Keratinocytes had a perinuclear halo. Keratinocyte diameter differed between cetacean suborders and amongst species. Melanophage clusters were common in most cetacean species. CONCLUSIONS: The widespread presence of melanin and the unexpectedly high number of melanophages may constitute a unique photoprotective trait of cetaceans and could reflect primitive adaptations to their environment and to their obligate marine-bound life.

Transformation of the genital epithelial tract occurs early in California sea lion development.

An unusually high prevalence of metastatic urogenital carcinoma has been observed in free-ranging California sea lions stranded off the coast of California in the past two decades. No cases have been reported for sea lions in the relatively unpolluted Gulf of California. We investigated occurrence of genital epithelial transformation in 60 sea lions (n=57 pups and 3 adult females) from the Gulf of California and examined whether infection by a viral pathogen previously found to be associated with urogenital carcinoma accounted for such alterations. We also explored the contribution of MHC class II gene expression on transformation. Cellular alterations, such as squamous cell atypia (ASC), atypical squamous cells of undetermined significance (ASCUS) and low-grade squamous intraepithelial lesions were observed in 42% of the pups and in 67% of the adult females. Normal genital epithelium was more common in male than female pups. ASC was five times more likely to occur in older pups. Epithelial alterations were unrelated to infection by the potentially oncogenic otarine type I gammaherpesvirus (OtHV-1), but ASCUS was more common in pups with marked and severe inflammation. Expression of MHC class II DRB loci (Zaca DRB-D) by peripheral antigen-presenting leucocytes showed a slightly 'protective' effect for ASC. We propose that transformation of the California sea lion genital epithelium is relatively common in young animals, increases with age and is probably the result of infection by an unidentified pathogen. Expression of a specific MHC class II gene, suggestive of presentation of specific antigenic peptides to immune effectors, appears to lower the risk of transformation. Our study provides the first evidence that epithelial transformation of the California sea lion genital tract is relatively common, even from an early age, and raises questions regarding differences in sea lion cancer-detection and -repair success between geographical regions.