Ecology of marine blooming bacteria

Abstract

Marine prokaryotes are fundamental to all biological and ecological processes in the ocean and are key drivers of global biogeochemical cycles. Prokaryotic communities comprise thousands of diverse taxa that undergo continuous successions across temporal and spatial gradients shaped by environmental variability. Occasionally, a single taxon may dominate the community —a phenomenon referred to as a “bloom”— potentially playing a disproportionate role in maintaining essential ecosystem functions. Despite their ecological significance, many aspects of the ecology of blooming taxa remain poorly understood, including their recurrence, specific triggering factors, and taxonomic diversity. This thesis aims to enhance our understanding of blooming bacterial taxa. To this end, we first used insights derived from the Blanes Bay Microbial Observatory (BBMO), a coastal long-term monthly metabarcoding time series in the NW Mediterranean Sea. Our analysis identified a limited number of taxa capable of exhibiting bloom-like behavior (ca. 1% of the total diversity), which belonged predominantly to the Flavobacteriales and Pseudomonadales, known copiotrophic orders. Despite the monthly sampling interval, we observed blooms at an average frequency of 4.6±1.9 times per year, considering both the 0.2–3 μm and 3–20 μm size fractions. No consistent association was found between environmental changes and the occurrence of blooms, but a marked increase in blooming events was observed during the period when the harbor near the BBMO site was restored—particularly within the 3–20 μm bacterioplankton size fraction (Chapter I). The absence of a strong link between environmental variability and blooming events may be due to the relatively sparse monthly sampling resolution. To overcome this limitation, we conducted a short twice-daily frequency sampling at the BBMO, which revealed that bloom events are frequent, transient and typically lasting only 24–48 hours (Chapter II). These findings challenge conventional assumptions, given that marine prokaryotes are generally thought to exhibit low in situ growth rates of around 1 d-1. Furthermore, these ephemeral blooms were sometimes associated with marked increases in heterotrophic activity, indicating that they can significantly alter community function. The rapid emergence of bloomers within such short time frames, and the unclear link with environmental parameters, drove us to test experimentally some of the insights observed in the first two chapters, in the following ones. We assessed the growth potential (i.e. the maximal growth rates in the absence of limiting factors) of individual taxa using manipulation experiments in which known growth-limiting factors—such as predation, nutrient limitation, and viral lysis—were reduced. These experiments revealed a wide spectrum of growth rates, ranging from 0.1 to 10 d-1, indicating 17 that certain taxa can indeed transition from rare to dominant in just 24–48 hours (Chapter III). Furthermore, using another set of manipulation experiments (Chapter IV), we tested whether different carbon sources selected for different bacteria with the potential to bloom, and we found that the same taxa (e.g., Alteromonas and Rhodobacteraceae) responded consistently to the different additions, yet their success in dominating the community depended on the carbon source. Additionally, priority effects—where taxa that are relatively abundant at the beginning could have a competitive advantage over rarer ones— also influenced the response. Overall, this thesis contributes to the understanding of marine bacterial bloomers by elucidating their taxonomic composition, temporal trends, growth dynamics, and potential functional roles. Our findings suggest that these taxa may contribute significantly to ecosystem resilience by rapidly responding to both anthropogenic and natural environmental perturbations.