Abstract

Microbial communities are of considerable significance for biogeochemical processes, for the health of both animals and plants, and for biotechnological purposes. A key feature of microbial interactions is the exchange of nutrients between cells. Isotope labelling followed by analysis with secondary ion mass spectrometry (SIMS) can identify nutrient fluxes and heterogeneity of substrate utilisation on a single cell level. Here we present a novel approach that combines SIMS experiments with mechanistic modelling to reveal otherwise inaccessible nutrient kinetics. The method is applied to study the onset of a synthetic mutualistic partnership between a vitamin B12-dependent mutant of the alga Chlamydomonas reinhardtii and the B12-producing, heterotrophic bacterium Mesorhizobium japonicum, which is supported by algal photosynthesis. Results suggest that an initial pool of fixed carbon delays the onset of mutualistic cross-feeding; significantly, our approach allows the first quantification of this expected delay. Our method is widely applicable to other microbial systems, and will contribute to furthering a mechanistic understanding of microbial interactions.

Highlights

  • Microbial communities underpin many globally important processes, from biogeochemical cycles [1] and the ecology of aquatic [2] and terrestrial food webs [3,4], to wastewater treatment [5,6] and the health of agricultural soils [7]

  • While several studies have demonstrated mutualistic interaction between bacteria and algae mediated by nutrient exchange [36,37,40], none have integrated time-resolved secondary ion mass spectrometry (SIMS) with mechanistic modelling to elucidate nutrient kinetics, as we have done here

  • Our approach allows the quantification of nutrient kinetics that control the inception and temporal development of an algal-bacterial mutualism

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Summary

Introduction

Microbial communities underpin many globally important processes, from biogeochemical cycles [1] and the ecology of aquatic [2] and terrestrial food webs [3,4], to wastewater treatment [5,6] and the health of agricultural soils [7]. RAF’s contribution, including the laser microscopy, was funded by an Academy Fellow Grant from the Knut and Alice Wallenberg Foundation The funders did not play any role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript

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