From nets to networks: tools for deciphering phytoplankton metabolic interactions within communities and their global significance.

Our oceans are populated with a wide diversity of planktonic organisms that form complex dynamic communities at the base of marine trophic networks. Within such communities are phytoplankton, unicellular photosynthetic taxa that provide an estimated half of global primary production and support biogeochemical cycles, along with other essential ecosystem services. One of the major challenges for microbial ecologists has been to try to make sense of this complexity. While phytoplankton distributions can be well explained by abiotic factors such as temperature and nutrient availability, there is increasing evidence that their ecological roles are tightly linked to their metabolic interactions with other plankton members through complex mechanisms (e.g. competition and symbiosis). Therefore, unravelling phytoplankton metabolic interactions is the key for inferring their dependency on, or antagonism with, other taxa and better integrating them into the context of carbon and nutrient fluxes in marine trophic networks. In this review, we attempt to summarize the current knowledge brought by ecophysiology, organismal imaging, in silico predictions and co-occurrence networks using 'omics data, highlighting successful combinations of approaches that may be helpful for future investigations of phytoplankton metabolic interactions within their complex communities.This article is part of the theme issue 'Connected interactions: enriching food web research by spatial and social interactions'.

Complementary environmental analysis and functional characterization of lower glycolysis-gluconeogenesis in the diatom plastid.

Organic carbon fixed in chloroplasts through the Calvin-Benson-Bassham Cycle can be diverted towards different metabolic fates, including cyoplasmic and mitochondrial respiration, gluconeogenesis, and synthesis of diverse plastid metabolites via the pyruvate hub. In plants, pyruvate is principally produced via cytoplasmic glycolysis, although a plastid-targeted lower glycolytic pathway is known to exist in non-photosynthetic tissue. Here, we characterized a lower plastid glycolysis-gluconeogenesis pathway enabling the direct interconversion of glyceraldehyde-3-phosphate and phospho-enol-pyruvate in diatoms, ecologically important marine algae distantly related to plants. We show that two reversible enzymes required to complete diatom plastid glycolysis-gluconeogenesis, Enolase and bis-phospho-glycerate mutase (PGAM), originated through duplications of mitochondria-targeted respiratory isoforms. Through CRISPR-Cas9 mutagenesis, integrative 'omic analyses, and measured kinetics of expressed enzymes in the diatom Phaeodactylum tricornutum, we present evidence that this pathway diverts plastid glyceraldehyde-3-phosphate into the pyruvate hub, and may also function in the gluconeogenic direction. Considering experimental data, we show that this pathway has different roles dependent in particular on day length and environmental temperature, and show that the cpEnolase and cpPGAM genes are expressed at elevated levels in high latitude oceans where diatoms are abundant. Our data provide evolutionary, meta-genomic and functional insights into a poorly understood yet evolutionarily recurrent plastid metabolic pathway.