Microbial Biochemistry of Emerging Contaminants and Anthropogenic Organic Matter in the Atlantic and Southern Oceans

Abstract

[eng] The introduction of anthropogenic organic chemicals into the environment, particularly those exhibiting persistence, bioaccumulation, potential for long-range transport, and toxicity, poses a threat to the well-being of the Earth system. The global ocean, a vital component that sustains life, is especially vulnerable as it often serves as the main sink for these contaminants. In the marine environment, classic pollutants such as the polycyclic aromatic hydrocarbons (PAHs) and emerging contaminants like the organophosphate esters (OPEs) and the per- and polyfluoroalkyl substances (PFAS) compose the anthropogenic dissolved organic carbon (ADOC) pool. The fate of these compounds is governed by complex interactions between physicochemical and biological processes, with the marine microbial communities potentially playing a relevant role, as they do in the marine biogeochemical cycles. However, their role in processing background contaminant concentrations in the open ocean, as well as the effects of these compounds on marine microbes, remains poorly studied. This thesis explores the impact of background concentrations of organic contaminants—including PAHs, OPEs, and PFAS—on marine microbial communities and their role in the biodegradation of these pollutants in the global ocean. Focusing on remote regions like coastal Antarctica and the open ocean, the works presented in this thesis integrate chemical data on contaminant concentrations with compositional and functional data on marine microbial communities, as well as other physicochemical parameters, obtained from field measurements and experiments, to investigate the interactions between contaminants and microbial communities under real oceanic conditions. In coastal Antarctica, significant correlations were found between contaminant concentrations and microbial composition, highlighting complex biogeochemical controls at low contaminant levels. The results of this thesis provide the largest dataset on PAH and PFAS concentrations in coastal Antarctica, revealing substantial temporal and spatial variability linked to snowmelt and geographical features. They also show that PAH biodegradation is enhanced by snowmelt-induced bacterial activity, while microbial-mediated desulfurization may serve as a PFAS sink. In addition, aromatic hydrocarbon-degrading genes were identified across diverse marine microorganisms using a curated bioinformatic approach with metagenomic datasets, indicating a widespread potential for PAH biodegradation in temperate and tropical oceans. Assessment of the gene abundance and PAH concentrations showed a negative correlation with the low molecular weight fraction of the PAHs. Furthermore, background concentrations of PAHs were found to be a significant factor explaining variation in the bacterial community composition, together with other previously described environmental drivers of microbial communities such as temperature and nutrient concentrations. Field experiments revealed significant biodegradation of highly hydrophobic OPEs in the Atlantic Ocean, linked to increased bacterial protein production, marking the first open-ocean evidence of OPE biodegradation under natural conditions. This thesis demonstrates that concurrent characterization of organic contaminants and microbial communities through field-based measurements provides accurate insights into the complexity of real environmental conditions. It reveals that background levels of organic contaminants, while not the main drivers, have the potential to influence marine microbial communities significantly. Additionally, microbial degradation was observed to be a potential oceanic sink for emerging contaminants in the surface ocean. These findings highlight the need for further research on biodegradation rates and the impact of contaminants on marine biogeochemical cycles. Understanding these processes is essential for accurate risk assessments, especially given the rising release of anthropogenic compounds and the intensification of climate change-related stressors.

[cat] La introducció de compostos orgànics antropogènics derivats d'activitats humanes en el medi ambient, inclosos els contaminants orgànics persistents i els contaminants emergents, com els hidrocarburs aromàtics policíclics (HAP), els èsters organofosforats (OPE) i les substàncies per- i polifluoroalquilades (PFAS), representa una amenaça per als ecosistemes marins de l’oceà global. Aquests contaminants interactuen amb les comunitats microbianes marines, podent alterar els cicles biogeoquímics. No obstant això, l'abast del seu impacte, així com el paper dels microbis en la determinació del destí dels contaminants mitjançant la degradació o altres processos, continua sent poc conegut. Aquesta tesi investiga els efectes dels nivells de fons de contaminants en els microbis marins i el seu possible paper en la biodegradació d'aquests compostos, centrant-se en regions remotes com la costa de l'Antàrtida i l'oceà obert. Per a això, integra dades químiques amb dades de la composició i funció de les comunitats microbianes, així com altres paràmetres fisicoquímics obtinguts a partir de mesuraments de camp i experiments realitzats durant diferents campanyes de mostreig. Els conjunts de dades obtingudes van ser analitzats utilitzant eines d'anàlisis de dades, proves estadístiques i programari de bioinformàtica. Aquesta tesi demostra que la caracterització simultània de contaminants orgànics i comunitats microbianes mitjançant mesuraments de camp proporciona nou coneixement sobre la complexitat dels processos que es desenvolupen baix condicions ambientals reals. Revela que els nivells de fons de contaminants orgànics, encara que no siguin els principals impulsors, poden influir significativament en les comunitats microbianes marines. A més, es va observar que la degradació microbiana podria actuar com un embornal oceànic per a contaminants emergents en la superfície de l'oceà. Aquestes troballes ressalten la necessitat de continuar investigant tant les taxes de biodegradació microbiana com l'impacte dels contaminants sobre les comunitats microbianes i, per tant, en els cicles biogeoquímics marins. Comprendre aquests processos és essencial per a realitzar avaluacions de risc precises, especialment davant l'augment en l'alliberament de compostos antropogènics i la intensificació dels factors d'estrès ambiental derivats del canvi climàtic.