Fifteen-year microbiome survey of endangered killer whales (Orcinus orca) reveals declining diversity and population differences

The endangered Southern Resident killer whale (Orcinus orca) (SRKW) population is burdened by multiple anthropogenic stressors with limited non-invasive approaches for health surveillance. The gut microbiome is interconnected with host physiology and can be characterized using remotely collected fecal samples, creating unique opportunities to integrate environmental and individualized host-associated features of health. In this study, we used fecal samples collected over a 15-year period (2005-2019) from 77% of the living, wild SRKW population (56 individuals, 1-17 time points per individual), as well as fecal samples from the conspecific Northern and Alaska Resident killer whale populations, to characterize distal gut microbiota structure and genomic composition. SRKW microbiotas were individualized and distinct from those of the nearby Northern and Alaska Resident populations, both of which exhibit consistently higher fecundity and survivorship. During the study period, SRKW fecal microbiota species richness declined, despite stability over periods of time less than or equal to 1 year. Several potential bacterial pathogens, such as Fusobacterium spp., achieved dominance in the fecal microbiotas of SRKW individuals sampled within 6 months of death. These findings demonstrate the feasibility and value of harnessing non-invasively collected fecal samples and microbiome profiles for longitudinal killer whale health surveillance.