Mechanisms and Rates of Bacterial Colonization of Sinking Aggregates

Abstract

Quantifying the rate at which bacteria colonize aggregates is a key to understanding microbial turnover of aggregates. We used encounter models based on random walk and advection-diffusion considerations to predict colonization rates from the bacteria's motility patterns (swimming speed, tumbling frequency, and turn angles) and the hydrodynamic environment (stationary versus sinking aggregates). We then experimentally tested the models with 10 strains of bacteria isolated from marine particles: two strains were nonmotile; the rest were swimming at 20 to 60 m s ؊1 with different tumbling frequency (0 to 2 s ؊1 ). The rates at which these bacteria colonized artificial aggregates (stationary and sinking) largely agreed with model predictions. We report several findings. Bacteria colonize marine aggregates where they grow and are preyed upon. Bacteria typically occur on aggregates in concentrations that are orders of magnitude higher than in the ambient water (10,11,40). They cause aggregates to solubilize and remineralize, apparently at high rates (1, 36, 37). Even if microbial processes on aggregates account for only a small fraction of the total microbial activity in the water column (4, 40), seepage of dissolved organic matter from degrading aggregates can affect microbial processes even outside the aggregates. For example, the few available estimates of leakage rates from aggregates suggest that aggregates may be quantitatively significant dissolved organic matter sources for free bacteria and that the solute plumes trailing behind sinking aggregates may be important sites of bacterial growth (19,23,39). Thus, marine aggregates are not only sinking vehicles but also important components of the pelagic food webs. Bacterial activities on aggregates are key to understanding this role.In resolving the population dynamics of bacteria on aggregates one needs to consider the rate at which bacteria colonize the aggregates. Several studies have described the succession of microbes on aggregates (19,26,36,41,43), but few have examined the colonization process at a relevant-i.e., short (minutes)-time scale (15), and none have adequately considered the effect of the flow environment on colonization. A significant fraction of pelagic bacteria are motile (15,18,30), and simulation models have shown that motility and chemosensing capability are important for colonization, even of sinking aggregate (21, 23). Here we develop encounter models to predict colonization rates based on observed motility patterns of the bacteria and the hydrodynamic environments. We then compare model predictions with empirical measurements by using artificial aggregates. MATERIALS AND METHODS Models of colonization.The change in the number of bacteria on an aggregate due to colonization, dN/dt, equals the transport of bacteria toward the aggregate, F, which in turn depends on the ambient concentration of bacteria, C,where ␤ is the "encounter rate kernel," i.e., the imaginary volume of water from which the aggregate "collects" bacteria per unit time. ...

Carbon and nitrogen fluxes associated with the cyanobacterium Aphanizomenon sp. in the Baltic Sea

“…In this study, modeled NH 4 þ concentrations inside Aphanizomenon colonies were 37-fold higher than that of the bulk (Figure 6), and such colonies could potentially be a microenvironment favorable for growth of heterotrophic bacteria. Many pelagic bacteria are motile, show chemotaxis toward aggregate nutrient sources, and their colonization times are in the order of minutes (Kiørboe et al, 2002). However, bacterial colonization of Aphanizomenon colonies was low (data not shown).…”

Carbon, nitrogen and O2 fluxes associated with the cyanobacterium Nodularia spumigena in the Baltic Sea

“…N. spumigena is usually colonized by a diverse community of bacteria exhibiting high ecto-enzymatic activities (Hoppe, 1981;Stoecker et al, 2005;Tuomainen et al, 2006), and a significant fraction of the primary production, measured by use of H 14 CO 3 in N. spumigena colonies from the Baltic Sea, was incorporated into the associated bacteria (Hoppe, 1981). Many pelagic bacteria are motile, show chemotaxis and their colonization rates of particles are in the order of minutes (Kiørboe et al, 2002). The nitrogen sources leaking from Nodularia colonies may sustain growth of other biota when bulk concentrations of dissolved inorganic nitrogen are low.…”

Effects of starvation on aggregate colonization and motility of marine bacteria

“…A 1 ml aliquot of the ambient bacteria was also counted at the start and end of the colonization experiment. The model of Kiørboe et al (2002) was fitted to the data to estimate diffusivities (D m ) and detachment rates (δ m ):…”

“…Convective heating created a small net flow in the chambers, which was corrected for in the analysis using additional tracks of abiotic particles in the field of view. The average 3-dimensional speed of the bacterium was estimated as (3/2) 1 ⁄ 2 multiplied by the corrected 2-dimensional speed, and the empirically derived diffusivity (D e ) was calculated according to Kiørboe et al (2002): (2) where u is the swimming velocity; τ is the run length; and α is the mean cosine of the angles between 2 successive runs. Additionally, swimming speed data were used to generate frequency distributions for both starved and fed treatments.…”

“…Wei & Bauer (1998) reported that prolonged starvation in the terrestrial bacterium Rhizobium meliloti resulted in a graded response, ranging from loss or modification of flagella to inactivation of the flagellar motor. Kiørboe et al (2002) estimated that the search time for a bacterium to encounter an aggregate in the upper ocean was 0.02 to 12 d, with a median of 0.4 d; thus, most bacteria should reach an aggregate within 1 d of continuous searching. However, this estimation assumes constant diffusivity and velocity for well-fed, exponentially growing bacteria .…”