Invisible threats to oceans (InTO): assessing the combined toxicity effects of emerging anthropogenic pollutants on microbial communities

Abstract

Marine environments near populated and tidal convergence zones accumulate pollutants, many of which are toxic to marine life. The impact of these pollutants on marine microorganisms threatens the biochemical balance of the oceans and can induce cascading changes throughout the food chain, prompting urgent investigation. Plastics are of particular concern due to their persistence in the ocean, their accumulation of persistent organic pollutants (POPs), and their role in carrying and transporting marine microbial communities termed ‘plastispheres’. In this thesis, the combined impact of plastics and POPs on these marine microbial communities was therefore studied to reveal the impact of this interaction on essential microbial metabolic processes. In Chapter 2, marine microbial communities extracted from beached plastics were grown on pristine low-density polyethylene (LDPE) for three and seven days. Metagenomic analysis revealed increased microbial abundance over time, and a prevalence of potential pathogens. Metaproteomic analysis identified proteins involved in bacterial attachment, cell-cell interaction, biofilm maintenance, and antioxidant production, along with limited proteins related to pollutant biodegradation and virulence. In Chapter 3, the secretome of the representative marine bacterium Epibacterium mobile was studied after short exposure to the organic UV-filters benzophenone-3 (BP3), and ethylhexyl methoxycinnamate (EHMC), a more commonly used UV-filter. E. mobile was exposed to each UV-filter separately, and the proteins secreted into the medium were examined. Analysis of protein yields and contamination highlighted challenges inherent to the analysis of the secretome. However, regardless of technical limitations, growth and metaproteomics data showed that EHMC elicits a markedly different response in E. mobile than BP3. Finally, in Chapter 4, a nascent marine plastisphere was exposed to 5 mg/L EHMC, and analysed for metabolic impacts of co-pollution on the plastisphere. Metagenomic analysis of the plastisphere after EHMC exposure revealed a decline in growth and activity of a genera associated with pollutant biodegradation, and an increase in the growth and activity of other genera containing pathogenic species. EHMC exposure also triggered a stress response and the regulation of nitrogen respiration proteins, suggesting an inhibition of aerobic processes. In the marine environment, co-pollutants like EHMC may therefore impact plastic persistence by inhibiting core metabolic processes, as well as increasing the prevalence of potentially pathogenic bacteria, further threatening public health. Furthermore, this research indicates that combined pollution amplifies toxicity towards marine microorganisms, posing additional risks to microbial communities, and their biogeochemical processes. This thesis demonstrates that combined pollution represents a significant, multifaceted threat to marine environments. Left unaddressed, these interactions could increase the hazards associated with the marine environment, compromise essential ecosystem services, and perpetuate the accumulation of pollutants. Continued efforts to mitigate pollution and monitor its effects on microbial communities will be critical to safeguarding the health of marine ecosystems and, by extension, the planet.