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 metatranscriptome 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 trehalose is produced by the nitrogen-fixing cyanobacterium Crocosphaera, likely to store energy for nighttime metabolism. Together, paired measurements of particulate metabolites and transcripts resolve strategies that microbes use to manage daily energy and redox oscillations and highlight dynamic metabolites with cryptic roles in marine microbial ecosystems. IMPORTANCE Fueled by light, phytoplankton produce the organic matter that supports ocean ecosystems and carbon sequestration. Ocean change impacts microbial metabolism with repercussions for biogeochemical cycling. As the small molecule products of cellular metabolism, metabolites often change rapidly in response to environmental conditions and form the basis of energy and nutrient management and storage within cells. By pairing measurements of metabolites and gene expression in the stratified surface ocean, we reveal strategies of microbial energy management over the day-night cycle and hypothesize that oscillating metabolites are important substrates for dark respiration by phytoplankton. These high-resolution diel measurements of in situ metabolite concentrations form the basis for future work into the specific roles these compounds play in marine microbial communities.

Glycine betaine uptake and metabolism in marine microbial communities

“…Except for GBT, other metabolites were quantified using the response factors and response factor ratios of authentic standards spiked into water and into representative pooled samples, as described in Boysen et al . (2021).…”

Linkages Among Dissolved Organic Matter Export, Dissolved Metabolites, and Associated Microbial Community Structure Response in the Northwestern Sargasso Sea on a Seasonal Scale

“…Advanced technologies such as ultrahigh resolution mass spectrometry enable detection of DOM composition at the molecular or compound level, in addition to specific biomolecules such as TDAA ( Sleighter and Hatcher, 2008 ; Lechtenfeld et al, 2014 ; Kido Soule et al, 2015 ; Medeiros et al, 2015 ; Osterholz et al, 2016 ). Using these techniques, metabolomics, including both particulate and dissolved metabolomics, has primarily been applied to marine culture studies ( Baran et al, 2010 ; Fiore et al, 2015 ; Longnecker et al, 2015 ; Kashfi et al, 2020 ), with more limited applications to field samples ( Durham et al, 2019 ; Johnson et al, 2020 ; Boysen et al, 2021 ; Heal et al, 2021 ). However, seasonal changes of dissolved metabolites in the marine environment are rarely studied.…”

Deciphering Metabolic Currencies That Support Marine Microbial Networks

“…Because sulfate concentration is high in seawater (∼28 mM), phytoplankton can leverage this readily available inorganic nutrient to shunt excess reducing power from photosynthesis, and bacterial associates use resulting organic sulfur outputs for growth. Indeed, phytoplankton-derived sulfur metabolites display day-night rhythms in abundance consistent with this idea ( 17 , 18 ). Regulation of microbial sulfur metabolism is a current gap in our understanding of marine sulfur biogeochemistry that we are now poised to address.…”

“…We then bioinformatically inferred metabolic pathways and tracked sulfonate dynamics in natural microbial communities of the North Pacific ( 17 ). So far, field observations suggest sulfonate production in phytoplankton is regulated by both light and nutrient availability ( 17 , 18 , 21 ), ideas that we are exploring back in the lab.…”