Aquatic polymers can drive pathogen transmission in coastal ecosystems

Abstract

Gelatinous polymers including extracellular polymeric substances (EPSs) are fundamental to biophysical processes in aquatic habitats, including mediating aggregation processes and functioning as the matrix of biofilms. Yet insight into the impact of these sticky molecules on the environmental transmission of pathogens in the ocean is limited. We used the zoonotic parasite Toxoplasma gondii as a model to evaluate polymer-mediated mechanisms that promote transmission of terrestrially derived pathogens to marine fauna and humans. We show that transparent exopolymer particles, a particulate form of EPS, enhance T. gondii association with marine aggregates, material consumed by organisms otherwise unable to access micrometre-sized particles. Adhesion to EPS biofilms on macroalgae also captures T. gondii from the water, enabling uptake of pathogens by invertebrates that feed on kelp surfaces. We demonstrate the acquisition, concentration and retention of T. gondii by kelp-grazing snails, which can transmit T. gondii to threatened California sea otters. Results highlight novel mechanisms whereby aquatic polymers facilitate incorporation of pathogens into food webs via association with particle aggregates and biofilms. Identifying the critical role of invisible polymers in transmission of pathogens in the ocean represents a fundamental advance in understanding and mitigating the health impacts of coastal habitat pollution with contaminated runoff.

Keywords: Toxoplasma gondii; extracellular polymeric substances; marine transmission; sea otter; transparent exopolymer particles; zoonotic pathogen.

Figure 1.

Two mechanisms are proposed whereby polymers can mediate transmission of terrestrial pathogens in coastal ecosystems (depicted here for a model zoonotic protozoan parasite, Toxoplasma gondii). Pelagic polymers such as TEPs may enhance the association of pathogens with sinking macroaggregates (shown in this study), while benthic exopolymer substances (EPS) can trap pathogens within sticky biofilms [22]. Both mechanisms are likely to increase the probability of pathogen entry into the marine food web through aggregate-consuming invertebrates such as bivalves or surface scraping molluscs such as snails. Ingestion of contaminated prey items can then lead to pathogen exposure in susceptible hosts, including threatened California sea otters and humans.

Figure 2.

Proportion of Toxoplasma gondii oocysts recovered after 24 h from the aggregate-rich fractions of seawater with differing TEP concentrations in (a) experiment 1, where seawater was spiked with increasing concentrations of alginic acid (AA; a source of TEP), and (b) experiment 2, containing seawater samples collected on different dates with variable but naturally derived TEP mixtures and concentrations. TEP concentrations are indicated in parentheses as μg xanthan gum equivalent l⁻¹. In both experiments, significantly higher numbers of oocysts were associated with aggregates as TEP concentrations in the water increased (negative binomial regression p < 0.001). Error bars denote 1 s.d. from the mean (n = 5). Black bars denote seawater; grey bars, filtered seawater.

Figure 3.

(a,b) Toxoplasma gondii oocyst (arrows) associated with a TEP-embedded aggregate under (a) DAPI epifluorescence and (b) DAPI and bright field illumination, revealing TEP (blue staining). (c) Section of alcian blue-stained kelp showing emanating EPS fibres. (d) Ventral surface of turban snail with enlargement of scraping radula. (e,f) Toxoplasma gondii oocyst (arrows) in snail faeces under (e) DAPI epifluorescence only and (f) combined DAPI and bright field illumination, revealing EPS/TEP (blue) entrained in faecal material.

Figure 4.

Numbers of Toxoplasma gondii oocysts detected in snail faeces over 14 days in which snails were maintained in an oocyst-free environment. Following the 24 h exposure period (time 0), oocysts were present in faeces at concentrations 150-fold greater than in the spiked seawater and were defecated for 10 days after removal from T. gondii-contaminated water. Oocysts were not detected in snail faeces on days 11–14 following snails’ removal from contaminated water. Error bars denote 1 s.d. from the mean (n = 6).