Combining SIMS and mechanistic modelling to reveal nutrient kinetics in an algal-bacterial mutualism

• Published in: PloS one 2021-05, Vol.16 (5), p.e0251643-e0251643
• Main Authors: Laeverenz Schlogelhofer, Hannah, Peaudecerf, François J, Bunbury, Freddy, Whitehouse, Martin J, Foster, Rachel A, Smith, Alison G, Croze, Ottavio A
• Format: Article
• Language: English
• Subjects: Activated carbon; Algae; Analysis; Axenic culture; Bacteria; Bacterial growth; Biological Physics; Biology and Life Sciences; Carbon; Carbon sequestration; Carrying capacity; Cell culture; Cell density; Chlamydomonas reinhardtii - metabolism; Chlamydomonas reinhardtii - microbiology; Dissolved organic carbon; Dynamics; Ecosystems and species history; Ekosystem och arthistoria; Environmental conditions; Experiments; Exudation; Fluxes; Genetic drift; Genetic engineering; Glycerol; Growth rate; Hybridization; Isotope analysis; Isotopes; Labeling; Laboratories; Mass spectrometry; Mass spectroscopy; Mesorhizobium - genetics; Mesorhizobium - metabolism; Metabolism; Metabolites; Microbiota (Symbiotic organisms); Microorganisms; Models, Biological; Multidisciplinary; Mutation; Mutualism; Nutrients; Optimization; Parasitism; Photosynthesis; Phylogeny; Physical Sciences; Physics; Plant sciences; Population growth; Research and Analysis Methods; Respiration; rRNA 16S; Scientific imaging; Secondary ion mass spectrometry; Spectroscopy; Symbiosis; Symbiosis - physiology; Syntrophism; Vitamin B 12 - metabolism; Yeast; Yeasts
• ISSN: 1932-6203; 1932-6203
• DOI: 10.1371/journal.pone.0251643

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.