Microscale advection governs microbial growth and oxygen consumption in macroporous aggregates

• DOI: 10.1128/msphere.00185-24
• Publication Date: 2024-03-26T13:11:57Z
• Authors: Rachel Shen; Benedict Borer; Davide Ciccarese; M. Mehdi Salek; Andrew R. Babbin
• Keywords: microbial aggregates; 570; 0303 health sciences; 03 medical and health sciences; 550; diffusion limitation; advective mass-transport; mass transport; biofilm establishment; Microbiology; QR1-502; Research Article

ABSTRACT

Most microbial life on Earth is found in localized microenvironments that collectively exert a crucial role in maintaining ecosystem health and influencing global biogeochemical cycles. In many habitats such as biofilms in aquatic systems, bacterial flocs in activated sludge, periphyton mats, or particles sinking in the ocean, these microenvironments experience sporadic or continuous flow. Depending on their microscale structure, pores and channels through the microenvironments permit localized flow that shifts the relative importance of diffusive and advective mass transport. How this flow alters nutrient supply, facilitates waste removal, drives the emergence of different microbial niches, and impacts the overall function of the microenvironments remains unclear. Here, we quantify how pores through microenvironments that permit flow can elevate nutrient supply to the resident bacterial community using a microfluidic experimental system and gain further insights from coupled population-based and computational fluid dynamics simulations. We find that the microscale structure determines the relative contribution of advection vs diffusion, and even a modest flow through a pore in the range of 10 µm s −1 can increase the carrying capacity of a microenvironment by 10%. Recognizing the fundamental role that microbial hotspots play in the Earth system, developing frameworks that predict how their heterogeneous morphology and potential interstitial flows change microbial function and collectively alter global scale fluxes is critical.

IMPORTANCE Microbial life is a key driver of global biogeochemical cycles. Similar to the distribution of humans on Earth, they are often not homogeneously distributed in nature but occur in dense clusters that resemble microbial cities. Within and around these clusters, diffusion is often assumed as the sole mass-transfer process that dictates nutrient supply and waste removal. In many natural and engineered systems such as biofilms in aquatic environments, aggregates in bioremediation, or flocs in wastewater treatment plants, these clusters are exposed to flow that elevates mass transfer, a process that is often overlooked. In this study, we show that advective fluxes can increase the local growth of bacteria in a single microenvironment by up to 50% and shape their metabolism by disrupting localized anoxia or supplying nutrients at different rates. Collectively, advection-enhanced mass transport may thus regulate important biogeochemical transformations in both natural and engineered environments.