Absence of Staphylococcus aureus in wild populations of fish supports a spillover hypothesis

Staphylococcus aureus is a human commensal and opportunistic pathogen that can also colonise and cause disease in other animal species. In humans and livestock, where S. aureus is most studied, there is evidence that strains have different host specialisms. Recent studies have found S. aureus in many wild animals, including fish, whose physiologies and ecologies are very different to humans. However, it remains unclear whether S. aureus is adapted to and persisting within these species, or if its presence is due to repeated spillover from a source population. Distinguishing between these two scenarios is important for both public health and conservation. In this study we looked for evidence to support the hypothesis that the presence of S. aureus in fish is the result of spillover, through testing for the presence of S. aureus in fish that are isolated from likely source populations. We sampled 123 brown trout and their environment from 16 sites in the Scottish Highlands. All these sites are remote and have very low populations density of wild animal species known to carry S. aureus, but were selected to represent variable levels of exposure to humans, avian and livestock species. While our sampling methods readily detected S. aureus from the external and internal organs of a farmed fish, we did not detect S. aureus in any wild trout or their environment from any of the 16 sites. We sequenced 12 S. aureus isolates from the farmed fish. While they were all from clonal-complex 45, the genomic diversity was high enough to indicate repeated acquisition from a source population. In addition, the presence of a {varphi}Sa3 prophage containing a human immune evasion cluster indicates a recent history of these isolates within human populations. Taken together, our results support the presence of S. aureus in fish being due to spillover from other host populations, rather than the adaptation of S. aureus to aquaculture or fish populations. Given predictions that fish consumption will increase, more whole genome sequencing of S. aureus in aquaculture is needed to understand the presence of S. aureus in these environments and to mitigate the risk to fish and human health.