Nasopulmonary mites (Acari: Halarachnidae) as potential vectors of bacterial pathogens, including Streptococcus phocae, in marine mammals

Abstract

Nasopulmonary mites (NPMs) of the family Halarachnidae are obligate endoparasites that colonize the respiratory tracts of mammals. NPMs damage surface epithelium resulting in mucosal irritation, respiratory illness, and secondary infection, yet the role of NPMs in facilitating pathogen invasion or dissemination between hosts remains unclear. Using 16S rRNA massively parallel amplicon sequencing of six hypervariable regions (or "16S profiling"), we characterized the bacterial community of NPMs from 4 southern sea otters (Enhydra lutris nereis). This data was paired with detection of a priority pathogen, Streptococcus phocae, from NPMs infesting 16 southern sea otters and 9 California sea lions (Zalophus californianus) using nested conventional polymerase chain reaction (nPCR). The bacteriome of assessed NPMs was dominated by Mycoplasmataceae and Vibrionaceae, but at least 16 organisms with pathogenic potential were detected as well. Importantly, S. phocae was detected in 37% of NPM by nPCR and was also detected by 16S profiling. Detection of multiple organisms with pathogenic potential in or on NPMs suggests they may act as mechanical vectors of bacterial infection for marine mammals.

Fig 1. Plot of operational taxonomic units (OTUs) of bacteria from 8 pools of nasopulmonary mites infesting 4 southern sea otters (Enhydra lutris nereis) by taxonomic family.

Fig 2. Examples of pathology associated with nasopulmonary mite infestations in southern sea otters (Enhydra lutris nereis).

(A) Example rhinoscopic view of the nasopharynx from a live southern sea otter infested with nasopulmonary mites, showing abundant mucopurulent and variably hemorrhagic fluid surrounding adult nasopulmonary mites covering the ventral and lateral nasopharyngeal mucosa (Bar = 0.75 mm); (B) Diffusely inflamed, congested and mildly edematous nasopharyngeal mucosa in a necropsied sea otter with severe nasopulmonary mite infestation (Bar = 4 mm); (C) Example microscopic view of adult nasopulmonary mites attached to an inflamed, edematous and hemorrhagic nasopharyngeal mucosa (Hematoxylin and eosin stain, Bar = 250 μm).

Fig 3. Microscopic views of perinasal draining lymph nodes from southern sea otters (Enhydra lutris nereis) with nasopulmonary mite infestations.

(A) Chronically inflamed retropharyngeal lymph node with lymphatic dilation (top left) and marked expansion of the lymph node capsule by a mixed inflammatory infiltrate (left). (B) Inflamed axillary lymph node containing two dense clusters of bacterial cocci (putative streptococci) in the superficial cortex. Both sections hematoxylin and eosin stain, Bar = 100 μm (A) and 40 μm (B).