Porous marine snow differentially benefits chemotactic, motile, and non-motile 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 that bacterial motility is required for particle colonization and chemotaxis specifically benefits at higher settling velocities. We further explore the role of particle microstructure on the colonization efficiency of bacteria with different motility traits. We highlight that non-motile cells benefit disproportionally from the porous microstructure and are relatively enriched in the particle wake due to the efficient particle colonization of chemotactic and motile cells. Our results imply that although the chemotactic and motile bacteria benefit from the high nutrient availability when colonizing the particles, scavenging of these cells benefits the often oligotrophic, non-motile cells common among the planktonic community.Significance statementBacteria in the ocean rely on ephemeral nutrient patches from sinking marine particles, but attaching to these structures is challenging as particle settling rates often exceed bacterial swimming velocities and the numerically dominant marine bacteria are non-motile – posing an interesting paradox about the prominence of particle foraging. Here, we quantify the importance of chemotaxis and motility for the efficient colonization of marine particles and find that although chemotaxis provides a clear advantage, motility is the basic requirement for particle colonization. We expand this analysis to consider highly heterogeneous particle structures and find a disproportionate benefit for non-motile cells by facilitating a direct encounter with the particle surface and enriching non-motile microbes in the nutrient-rich particle plume.

Formation and emergent dynamics of spatially organized microbial systems

“…In terms of attachment success, theoretical studies suggest that motility can be a key factor in colonization of surfaces in aquatic environments, as motile bacteria are expected to have two to four orders of magnitude higher diffusion coefficients than non-motile cells, and therefore increased particle encounter rates [ 36 ]. Recent experimental studies in milli-fluidic devices using wild-type, motile but non-chemotactic, and non-motile mutant cells of a chemotactic model organism show that the former can colonize sparsely distributed nutritious particles first [ 37 ].…”

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).…”