Diel investments in metabolite production and consumption in a model microbial system

Mario Uchimiya,Mary Ann Moran,Arthur S Edison,William Schroer,Malin Olofsson

doi:10.1038/s41396-021-01172-w

Abstract

Organic carbon transfer between surface ocean photosynthetic and heterotrophic microbes is a central but poorly understood process in the global carbon cycle. In a model community in which diatom extracellular release of organic molecules sustained growth of a co-cultured bacterium, we determined quantitative changes in the diatom endometabolome and the bacterial uptake transcriptome over two diel cycles. Of the nuclear magnetic resonance (NMR) peaks in the diatom endometabolites, 38% had diel patterns with noon or mid-afternoon maxima; the remaining either increased (36%) or decreased (26%) through time. Of the genes in the bacterial uptake transcriptome, 94% had a diel pattern with a noon maximum; the remaining decreased over time (6%). Eight diatom endometabolites identified with high confidence were matched to the bacterial genes mediating their utilization. Modeling of these coupled inventories with only diffusion-based phytoplankton extracellular release could not reproduce all the patterns. Addition of active release mechanisms for physiological balance and bacterial recognition significantly improved model performance. Estimates of phytoplankton extracellular release range from only a few percent to nearly half of annual net primary production. Improved understanding of the factors that influence metabolite release and consumption by surface ocean microbes will better constrain this globally significant carbon flux.

Highlights

The transfer of organic carbon from phytoplankton to bacteria via a pool of labile dissolved compounds is a key process in global carbon cycling, involving up to a third of fixed carbon [1, 2]
This largely unconstrained flux can be traced to the difficulties inherent in characterizing labile organic molecules dissolved in surface seawater, such as short turnover times due to rapid bacterial uptake and low concentrations due to efficient scavenging
R. pomeroyi was inoculated into axenic T. pseudonana cultures growing under a naturally oscillating light:dark cycle

Summary

Introduction

The transfer of organic carbon from phytoplankton to bacteria via a pool of labile dissolved compounds is a key process in global carbon cycling, involving up to a third of fixed carbon [1, 2]. Estimates of the proportion of net primary production (NPP) released extracellularly range from 4 to 47% [3], and of the proportion of heterotrophic bacterial carbon demand supported by extracellular release from 2 to 50% [1]. In part, this largely unconstrained flux can be traced to the difficulties inherent in characterizing labile organic molecules dissolved in surface seawater, such as short turnover times due to rapid bacterial uptake and low concentrations due to efficient scavenging The dissolved organic carbon (DOC) link between marine phytoplankton and bacteria has long been of interest [6,7,8], identifying the specific metabolites responsible and measuring their flux is challenging

Methods

Results

Conclusion