Microscale insights into marine biogeochemical cycling: Linking microbial activity and mass transfer

Abstract

Microbial transformations are fundamental drivers of biogeochemical cycling in marine environments. While larger-scale processes undoubtedly shape marine microbial communities, the life of individual microorganisms is intricately governed by processes occurring at a much smaller scale, ranging from micrometers to millimeters. At these scales, the solute concentration available to the microbial community is influenced by the interplay between transport processes and microbial metabolism. However, our current understanding of microbially mediated biogeochemical processes within such microenvironments is still limited. The aim of this thesis was to study the interplay of mass transfer and microbial reaction rates to determine how they govern biogeochemical cycling in microenvironments. To gain insights into these processes, microfluidic techniques were developed and combined with modeling studies to quantify and explore microscale transport processes. The study in chapter 2 aimed to assess the role of oxic sandy sediments in removing anthropogenic nitrogen inputs to the continental shelves by quantifying the contribution of anoxic microenvironments in nitrogen loss. We used oxygen sensitive sensor particles in a microfluidic device to map oxygen production and consumption rates on the surface of individual sand grains. The results showed significant variability in oxygen production and consumption rates on individual sand grain surfaces, suggesting the formation of distinct microenvironments. Integration of microfluidic data into a two-dimensional single sand grain model revealed that the formation of anoxic microenvironments is controlled by solute supply and microbial oxygen production and consumption rates. Subsequently, a non-dimensional number derived from the model was used to estimate the volumes of anoxic microenvironments and calculate associated nitrogen loss. The findings indicated that nitrogen loss in the North Sea could be underestimated by approximately 40%. To further investigate the impact of flow on microscale transport processes and activity within microenvironments, we utilized oxygen-sensitive sensor particles in conjunction with advanced imaging techniques to simultaneously visualize oxygen concentrations and flow fields (chapter 3). The method proved highly effective in non-invasively visualizing the microscale transport processes in the boundary layer, allowing us to visualize oxygen concentrations within and around a model laboratory aggregate. We further show how this novel approach can be used in other marine microenvironments, examining the exchange processes facilitated by cilia on corals. The results show the importance of flow in determining oxygen concentrations and the potential for different microbial metabolisms in marine microenvironments. The activity of microorganisms residing in distinct microenvironments was investigated in chapter 4 using a newly developed microfluidic device for cultivating cells under well-defined solute concentrations. By cultivating marine bacteria under controlled oxic and anoxic conditions, we observed variable growth rates attributed to different energy yields from aerobic respiration and fermentation. Automated image segmentation revealed delayed morphological adaptations in response to changing oxygen concentrations. This study emphasizes the diversity within the microbial community residing in different microenvironments. The combined findings from this thesis show that microbial activity and behavior within seemingly uniform environments are influenced by microscale gradients of solute resulting from mass transport and microbial reaction rates. The work presented in this thesis, through microfluidics, imaging techniques, and modeling studies, highlights the intricate interplay of solute transport and microbial reaction rates, ultimately determining the solute availability in microenvironments. Microbial activity within these distinct microenvironments likely plays a key role in biogeochemical cycling in the oceans.