Dynamics of Bacterial Community Composition and Activity during a Mesocosm Diatom Bloom

Bacterial community composition, enzymatic activities, and carbon dynamics were examined during diatom blooms in four 200-liter laboratory seawater mesocosms. The objective was to determine whether the dramatic shifts in growth rates and ectoenzyme activities, which are commonly observed during the course of phytoplankton blooms and their subsequent demise, could result from shifts in bacterial community composition. Nutrient enrichment of metazoan-free seawater resulted in diatom blooms dominated by a Thalassiosira sp., which peaked 9 days after enrichment (’24 mg of chlorophyll a liter 21 ). At this time bacterial abundance abruptly decreased from 2.8 3 10 6 to 0.75 3 10 6 ml 21 , and an analysis of bacterial community composition, by denaturing gradient gel electrophoresis (DGGE) of PCR-amplified 16S rRNA gene fragments, revealed the disappearance of three dominant phylotypes. Increased viral and flagellate abundances suggested that both lysis and grazing could have played a role in the observed phylotype-specific mortality. Subsequently, new phylotypes appeared and bacterial production, abundance, and enzyme activities shifted from being predominantly associated with the 1.0-mm size fraction, indicating a pronounced microbial colonization of particles. Sequencing of DGGE bands suggested that the observed rapid and extensive colonization of particulate matter was mainly by specialized a-Proteobacteria- and Cytophagalesrelated phylotypes. These particle-associated bacteria had high growth rates as well as high cell-specific aminopeptidase, b-glucosidase, and lipase activities. Rate measurements as well as bacterial population dynamics were almost identical among the mesocosms indicating that the observed bacterial community dynamics were systematic and repeatable responses to the manipulated conditions. During phytoplankton blooms in the ocean, primary productivity and its processing by the food web create a heterogeneous environment of particulate, colloidal, and dissolved organic matter in a continuum of size classes and concentrations (2, 4, 35, 76). Major changes in organic matter concentration and composition are expected to occur at different stages of the bloom. The variations in the organic matter regime are typically accompanied by pronounced changes in bacterial abundance, productivity, ectohydrolase activities, and colonization of particles (48, 68). In one recent mesocosm experiment (68), growth rates, colonization, and enzyme activities generally increased following the peak of a diatom bloom but different enzymes were found to peak at different times. In principle, these changes could have occurred without major shifts in the phylogenetic composition of the bacterial community. Shifts in activity and surface attachment would represent plasticity in the bacterial phenotypes, with enzyme expression and growth being regulated in response to the available organic substrates. Alternatively, the observed changes could have resulted from community succession, with bacteria with inherently different metabolic capabilities predominating at different stages of the bloom. Species successions could then affect as well as reflect bacteria-organic matter coupling and the biogeochemical fate of the bloom. For instance, a dominance of bacteria specialized in colonizing and hydrolyzing phytoplankton detritus would greatly influence the biogeochemical transformation of the detritus. At the same time, free-living species adapted for efficiently utilizing dissolved organic matter could prevent largescale dissolved organic matter accumulation despite its high production rates typical in the blooms (35, 68). Consistent with the latter interpretation, Martinez et al. (41)