Multi‐omics analyses reveal the signatures of metabolite transfers across trophic levels in a high‐CO2 ocean

Abstract

AbstractAlthough the diverse impacts of elevated dissolved CO2 and warming on organisms within various trophic levels in marine food webs are well documented, we have yet to explore the biological links across different levels of biological organization from primary producers to secondary producers on an evolutionary time scale in a high‐CO2 ocean. Here, we cultured a model marine diatom Phaeodactylum tricornutum (primary producer) in predicted future high‐CO2 and/or warming conditions for ~ 1250 d with an experimental evolution approach and then fed them to the clam Coelomactra antiquata (secondary producer). We present an in‐depth multi‐omics analysis along the methylome (primary producer)–transcriptome (primary producer)–metabolome (primary producer)–metabolome (secondary producer) continuum. Our results showed that the downregulated terpenoid backbone biosynthesis in the methylome and transcriptome lead to decreased pyruvate levels and upregulation of some pathways (such as phenylalanine metabolism) in the metabolome of the primary producer in the long‐term warming conditions. These changes in metabolomic profile in the primary producer were then transferred to the secondary producer, resulting in changes in abundance of some metabolites, such as decreases in pyruvate, and in pyruvaldhyde (also known as methylglyoxal), and increases in 2‐hydroxylamino‐4,6‐dinitrotoluene. Our study provides a new insight into the molecular mechanisms underlying the trophic transfer from primary to secondary producers in a future high‐CO2 ocean and may provide more accurate projections of marine ecosystem services and functions over the next century.