Porous marine snow differentially benefits chemotactic, motile, and nonmotile bacteria

Abstract

Particulate organic carbon settling through the marine water column is a key process that regulates global climate by sequestering atmospheric carbon. The initial colonization of marine particles by heterotrophic bacteria represents the first step in recycling this carbon back to inorganic constituents—setting the magnitude of vertical carbon transport to the abyss. Here, we demonstrate experimentally using millifluidic devices that although bacterial motility is essential for effective colonization of a particle leaking organic nutrients into the water column, chemotaxis specifically benefits at intermediate and higher settling velocities to navigate the particle boundary layer during the brief window of opportunity provided by a passing particle. We develop an individual-based model that simulates the encounter and attachment of bacterial cells with leaking marine particles to systematically evaluate the role of different parameters associated with bacterial run-and-tumble motility. We further use this model to explore the role of particle microstructure on the colonization efficiency of bacteria with different motility traits. We find that the porous microstructure facilitates additional colonization by chemotactic and motile bacteria, and fundamentally alters the way non-motile cells interact with particles due to streamlines intersecting with the particle surface.

Physical structure and interstitial flows govern microbial life in microenvironments

“…For example, advective fluxes in a carbon-limited system may elevate the carbon supply such that the system becomes oxygen limited since their diffusivities often differ significantly. Oxygen 34 has a diffusion coefficient of 18×10 −10 m 2 s −1 whereas L-valine 35 , citrate 36 , and sucrose 37 have diffusion coefficients of 6.6, 5.9, and 4.8×10 −10 m 2 s −1 , respectively (or 2.7, 3 and 3.7 times lower than oxygen). Considering that the stoichiometry for aerobic respiration between oxygen and a six-carbon sugar such as citrate is 6:1, a small increase in carbon flux can rapidly result in a rapid depletion of oxygen if oxygen fluxes do not increase correspondingly.…”

“…5e). For example, porous marine snow that permits interstitial advective flows is colonized more efficiently by both motile and non-motile cells when compared to a rough or smooth surfaced particle 37 . However, while motile cells showed an average 10-fold increase in colonization for porous particles, this varied considerably for non-motile cells ranging from a negligible increase to an over 1000-fold increase.…”

“…We used a fluorescently tagged Pseudomonas aeruginosa PA14 that constitutively expresses a yellow fluorescent protein (eyfp) for all experiments 37 . We used Lennox lysogeny broth (5 g L −1 NaCl, BD Life Sciences, further abbreviated LB) media for overnight cultures and in the experiment and supplemented the overnight cultures with 300 µg/ml Trimethoprim (Trp) to avoid contamination.…”

Genome-resolved metagenomics reveals abundant nitrate reducers and partitioning of nitrite usage within global oxygen deficient zones

“…High NO 3 concentrations in ODZs may enable co-existence of these NO 3 reducer ecotypes, particularly since NO 3 is never depleted in the bulk ocean. Furthermore, abundant napA NO 3 reducers frequently carry motility and chemotaxis genes, which may facilitate particle colonization [77][78][79] and suggests a particle-associated lifestyle, whereas dominant narG NO 3 reducers are primarily non-motile (Figure 6b, S7b). The lack of motility among narG-containing organisms suggests a more planktonic lifestyle whereby these organisms are sustained by dissolved organic and inorganic nutrients.…”

Niche formation and metabolic interactions result in stable diversity in a spatially structured cyanobacterial community

“…The latter process remains relatively difficult to study due to lack of model systems and has been explored primarily through analysis of natural and bioreactor samples -usually in single-time points studies. These analyses have shown aggregates and granules to usually contain photosynthetic cyanobacteria and to comprise of a resident community of diverse microbes (7)(8)(9)(10)(11)(12)(13)(14). Where analysed, these communities are found to be distinct from the microbial composition of the surrounding environment (10,14).…”