Pathology, microbiology, and genetic diversity associated with Erysipelothrix rhusiopathiae and novel Erysipelothrix spp. infections in southern sea otters (Enhydra lutris nereis)

Authors: CHANG, RI - University Of California, Davis; MILLER, MELISSA - University Of California, Davis; TEKEDAR, HASAN - Mississippi State University; ROSE, DIVYA - Mississippi State University; Garcia, Julio; Lafrentz, Benjamin; Older, Caitlin; Waldbieser, Geoffrey - Geoff; POMARANSKI, ERIC - University Of California, Davis; SHAHIN, KHALID - University Of California, Davis; CAMUS, ALVIN - University Of Georgia; BATAC, FRANCESCA - California Department Of Fish & Game; BRYNE, BARBARA - University Of California, Davis; MURRAY, MICHAEL - Monterey Bay Aquarium; GRIFFIN, MATT - Mississippi State University; SOTO, ESTEBAN - University Of California, Davis

Submitted to: Frontiers in Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/11/2023
Publication Date: 2/1/2024
Citation: Chang, R.K., Miller, M., Tekedar, H.C., Rose, D., Garcia, J.C., Lafrentz, B.R., Older, C.E., Waldbieser, G.C., Pomaranski, E., Shahin, K., Camus, A.C., Batac, F., Bryne, B., Murray, M.J., Griffin, M.J., Soto, E. 2024. Pathology, microbiology, and genetic diversity associated with Erysipelothrix rhusiopathiae and novel Erysipelothrix spp. infections in southern sea otters (Enhydra lutris nereis). Frontiers in Microbiology. 14:1303235. https://doi.org/10.3389/fmicb.2023.1303235.
DOI: https://doi.org/10.3389/fmicb.2023.1303235

Interpretive Summary: Erysipelothrix species are zoonotic bacterial pathogens that can cause morbidity and mortality in mammals, fish, reptiles, birds, and humans. The bacterium was identified and cultured from six southern sea otters that had been necropsied to determine the cause of death. The pathology associated with Erysipelothrix spp. infections, genotypic diversity of the bacteria, antimicrobial sensitivity, and virulence of two novel Erysipelothrix spp. isolates were examined. Bacterial septicemia was a primary or contributing cause of death in five of the six cases and various pathology was noted among the six sea otters. Two of the recovered isolates were unique and whole genome sequencing revealed they represent a new Erysipelothrix species and a E. rhusiopathiae subspecies. The names Erysipelothrix enhydrae sp. nov. and Erysipelothrix rhusiopathiae ohloneorum ssp. nov. were proposed, respectively. Both isoaltes were confirmed to be virulent using a fish disease model. This is the first description of the pathology, microbial characteristics, and genetic diversity of Erysipelothrix isolates recovered from diseased southern sea otters, a federally-listed threatened species. Methods presented here can facilitate case recognition, aid characterization of Erysipelothrix spp. isolates, and illustrate assessment of virulence using fish models.

Technical Abstract: Erysipelothrix spp., including E. rhusiopathiae, are zoonotic bacterial pathogens that can cause morbidity and mortality in mammals, fish, reptiles, birds, and humans. We estimated the frequency of detection of these opportunistic pathogens in live and dead southern sea otters (SSO: Enhydra lutris nereis), described pathology associated with Erysipelothrix spp. infections, characterized the genotypic diversity and antimicrobial sensitivity of SSO isolates, and evaluated the virulence of two novel Erysipelothrix spp. isolates from SSOs using an in vivo fish model. From 1998 through 2021 Erysipelothrix spp. were isolated from only six of >500 necropsied SSOs, while no isolates were obtained from >120 live-sampled SSOs. Three of those cases were a pure culture isolation, while the other three were mixed cultures. Bacterial septicemia was a primary or contributing cause of death in five of the six cases. Other pathology observed in Erysipelothrix spp.-infected SSOs included suppurative lymphadenopathy, fibrinosuppurative arteritis with thrombosis and infarction, bilateral uveitis and endophthalmitis, hypopyon, petechia and ecchymoses, mucosal infarction, and suppurative meningoencephalitis and ventriculitis. Short to long slender Gram-positive or Gram-variable bacterial rods were identified within lesions, alone or in combination with other opportunistic bacteria. All six SSO isolates had the spaA isotype'three clustered with terrestrial animal spaA E. rhusiopathiae strains via multi-locus sequence analysiss, and one clustered with marine mammal spaA E. rhusiopathiae strains. Two isolates did not cluster with any known Erysipelothrix spp.; whole genome sequencing revealed a novel Erysipelothrix species and novel E. rhusiopathiae subspecies. We propose the names Erysipelothrix enhydrae sp. nov. and Erysipelothrix rhusiopathiae ohloneorum ssp. nov. respectively. The type strains are E. enhydrae UCD-4322-04 and E. rhusiopathiae ohloneorum UCD-4724-06 respectively. Laboratory injection of tiger barbs (Puntigrus tetrazona) as an in vivo model resulted in infection and mortality for the two novel Erysipelothrix spp. Antimicrobial testing suggests that Erysipelothrix strains from SSOs are more resistant to conventional antibiotics used to treat infections in humans and marine mammals than isolates obtained from fish and other animals, potentially posing additional risks with respect to human transmission and bacterial spread between animals. This is the first description of the pathology, microbial characteristics, and genetic diversity of Erysipelothrix isolates recovered from diseased SSOs, a federally-listed threatened species. Methods presented here can facilitate case recognition, help prevent zoonotic transmission, aid characterization of Erysipelothrix spp. isolates, and illustrate assessment of virulence using fish models.