Abstract

The ability of marine microbes to navigate towards chemical hotspots can determine their nutrient uptake and has the potential to affect the cycling of elements in the ocean. The link between bacterial navigation and nutrient cycling highlights the need to understand how chemotaxis functions in the context of marine microenvironments. Chemotaxis hinges on the stochastic binding/unbinding of molecules with surface receptors, the transduction of this information through an intracellular signalling cascade, and the activation and control of flagellar motors. The intrinsic randomness of these processes is a central challenge that cells must deal with in order to navigate, particularly under dilute conditions where noise and signal are similar in magnitude. Such conditions are ubiquitous in the ocean, where nutrient concentrations are often extremely low and subject to rapid variation in space (e.g. particulate matter, nutrient plumes) and time (e.g. diffusing sources, fluid mixing). Stochastic, biophysical models of chemotaxis have the potential to illuminate how bacteria cope with noise to efficiently navigate in such environments. At the same time, new technologies for experimentation allow for continuous interrogation -- from milliseconds through to days -- of bacterial responses in custom dynamic nutrient landscapes, providing unprecedented access to the behaviour of chemotactic cells in microenvironments engineered to mimic those cells navigate in the wild. These recent theoretical and experimental developments have created an opportunity to derive population-level uptake from single-cell motility characteristics in ways that could inform the next generation of marine biogeochemical cycling models.

Highlights

  • The fine-scale interactions between marine bacteria and both dissolved and particulate organic matter underpin marine biogeochemistry, thereby supporting productivity and influencing carbon storage and sequestration in the planet’s oceans (Azam, 1998)

  • A promising method for creating custom dissolved (DOM) nutrient landscapes utilizes the photo-release of caged chemoattractants (McCray and Trentham, 1989; Jasuja et al, 1999; Sagawa et al, 2014; Jikeli et al, 2015). Dissolved organic compounds such as the amino acid glutamate, which naturally occurs in coastal environments and acts as a chemoattractant for marine bacteria (Barbara and Mitchell, 2003; Duursma and Dawson, 2011), can be chemically appended using a “cage” molecule

  • While these results assume sampling through discrete time intervals, it will be important for future work to examine the role of continuous integration of ligand binding events (Mora and Nemenman, 2019), determine exactly how cells average measurements, and ascertain how noise propagates through the chemotaxis networks of different model organisms (Micali and Endres, 2019)

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Summary

INTRODUCTION

The fine-scale interactions between marine bacteria and both dissolved and particulate organic matter underpin marine biogeochemistry, thereby supporting productivity and influencing carbon storage and sequestration in the planet’s oceans (Azam, 1998). Bacterial Chemotaxis in Marine Microenvironments at the length scales relevant to individual microbes, the ocean is an intricate and dynamic landscape of nutrient patches, at times too small to be mixed by turbulence (Kiørboe, 2008; Stocker, 2012). Quantifying the influence of microscale dynamics in oceanic nutrient cycling hinges on (1) interrogating bacterial chemotaxis in realistic microenvironments for extended periods of time and (2) developing mathematical models that capture the essential features of chemotaxis in dilute, dynamic conditions. In this Perspective, we discuss recently developed experimental tools and mathematical frameworks for furthering our understanding of bacterial chemotaxis. We examine the various ways in which noise can enhance or degrade the sensitivity of bacterial navigation, and outline priorities for future research

BRIDGING THE TIMESCALES OF MOTILITY AND METABOLISM
NOISE IN BACTERIAL CHEMOTAXIS
BACTERIAL UPTAKE KINETICS IN STRUCTURED MICROENVIRONMENTS
PRIORITIES FOR FUTURE RESEARCH
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