Particulate metabolites and transcripts reflect diel oscillations of microbial activity in the surface ocean

Abstract

Light fuels photosynthesis and organic matter production by primary producers in the sunlit ocean. The quantity and quality of the organic matter produced influence community function, yet in situ measurements of metabolites, the products of cellular metabolism, over the diel cycle are lacking. We evaluated community level biochemical consequences of oscillations of light in the North Pacific Subtropical Gyre by quantifying 79 metabolites in particulate organic matter from 15 m every 4 h over 8 days. Total particulate metabolite concentration peaked at dusk and represented up to 2% of total particulate organic carbon (POC). The concentrations of 55/79 (70%) individual metabolites exhibited significant 24-h periodicity, with daily fold changes from 1.6 to 12.8, often greater than those of POC and flow cytometry-resolvable biomass, which ranged from 1.2 to 2.8. Paired metatranscrip-tome analysis revealed the taxa involved in production and consumption of a subset of metabolites. Primary metabolites involved in anabolism and redox maintenance had significant 24-h periodicity and diverse organisms exhibited diel periodicity in transcript abundance associated with these metabolites. Compounds with osmotic properties displayed the largest oscillations in concentration, implying rapid turnover and supporting prior evidence of functions beyond cell turgor maintenance. The large daily oscillation of trehalose paired with metatranscriptome and culture data showed that tre-halose is produced by the nitrogen-fixing cyanobacterium Crocosphaera, likely to store energy for nighttime metabolism. Together, paired measurements of particulate metabo-lites and transcripts resolve strategies that microbes use to manage daily energy and re-dox oscillations and highlight dynamic metabolites with cryptic roles in marine microbial ecosystems.

Francois Ribalet

Principal Research Scientist

My research interests include phytoplankton, climate change, population modeling and flow cytometry.