Microbial interactions govern marine biogeochemistry. These interactions are generally considered to rely on exchange of organic molecules. Here we report on a novel inorganic route of microbial communication, showing that algal-bacterial interactions between Phaeobacter inhibens bacteria and Gephyrocapsa huxleyi algae are mediated through inorganic nitrogen exchange. Under oxygen-rich conditions, aerobic bacteria reduce algal-secreted nitrite to nitric oxide (NO) through denitrification, a well-studied anaerobic respiratory mechanism. The bacterial NO is involved in triggering a cascade in algae akin to programmed cell death. During death, algae further generate NO, thereby propagating the signal in the algal population. Eventually, the algal population collapses, similar to the sudden demise of oceanic algal blooms. Our study suggests that the exchange of inorganic nitrogen species in oxygenated environments is a potentially significant route of microbial communication within and across kingdoms.

The lag phase is key in resuming bacterial growth, but it remains underexplored particularly in environmental bacteria. Here we use transcriptomics and ¹³C-labelled metabolomics to show that the lag phase of the model marine bacterium Phaeobacter inhibens is shortened by methylated compounds produced by the microalgal partner, Emiliania huxleyi. Methylated compounds are abundantly produced and released by microalgae, and we show that their methyl groups can be collected by bacteria and assimilated through the methionine cycle. Our findings underscore the significance of methyl groups as a limiting factor during the lag phase and highlight the adjustability of this growth phase. In addition, we show that methylated compounds, typical of photosynthetic organisms, prompt diverse reductions in lag times in bacteria associated with algae and plants, potentially favouring early growth in some bacteria. These findings suggest ways to accelerate bacterial growth and underscore the significance of studying bacteria within an environmental context.

Microalgae are key players in the ecology and biogeochemistry of our oceans. Efforts to implement genomic and transcriptomic tools in laboratory studies involving microalgae suffer from the lack of published genomes.

Coral reefs are marine biodiversity hotspots that provide a wide range of ecosystem services ¹ . They are reservoirs of bioactive metabolites, many produced by microorganisms associated with reef invertebrate hosts ² . However, for the keystone species of coral reefs—the reef-building corals—we still lack a systematic assessment of their microbially encoded biosynthetic potential and the molecular resources at stake due to the alarming decline in reef biodiversity. Here we analysed microbial genomes reconstructed from 820 reef-building coral samples of three representative coral genera collected at 99 reefs across 32 islands throughout the Pacific Ocean ( Tara Pacific expedition) ³ . By contextualizing our analyses with the microbiomes of other reef species, we found that only 10% of the 4,224 microbial species and less than 1% of the 645 species exclusively identified in Tara Pacific samples had genomic information available. Furthermore, the biosynthetic potential of reef-building coral microbiomes rivalled or surpassed that of traditional natural product sources such as sponges. Among the biosynthetically rich bacteria in the reef microbiome, we identified new groups of Acidobacteriota that encode previously unknown enzymology, in turn opening promising avenues for functional protein engineering. Together, this study underscores the importance of conserving coral reefs as vital reservoirs of molecular diversity.

Bacterial signals control the development of marine algae, yet the molecular basis of these cross-kingdom interactions remains largely unknown. Thallusin is the paradigmatic case: isolated in 2005, it induces rhizoid and cell wall formation in the green seaweed Ulva at picomolar concentrations, but its biosynthesis has remained elusive for two decades. Comparative genomics across five bacterial phyla identifies a conserved set of genes - the eustigmatophyte bacterial operon ( ebo ) - as determinants of thallusin biosynthesis. Isotope labeling, heterologous expression, and gene deletion in Stieleria maiorica show that the aromatic scaffold derives from a cyclitol precursor and L-aspartate, with subsequent prenylation and cyclization. Searching 124,295 prokaryotic genomes identifies producers in eleven bacterial lineages, including soil cyanobacteria, establishing thallusin as a widespread cross-kingdom signal reaching beyond the ocean.