About half the carbon fixed by phytoplankton in the ocean is taken up and metabolized by marine bacteria, a transfer that is mediated through the seawater dissolved organic carbon (DOC) pool. The chemical complexity of marine DOC, along with a poor understanding of which compounds form the basis of trophic interactions between bacteria and phytoplankton, have impeded efforts to identify key currencies of this carbon cycle link. Here, we used transcriptional patterns in a bacterial-diatom model system based on vitamin B 12 auxotrophy as a sensitive assay for metabolite exchange between marine plankton. The most highly up-regulated genes (up to 374-fold) by a marine Roseobacter clade bacterium when cocultured with the diatom Thalassiosira pseudonana were those encoding the transport and catabolism of 2,3-dihydroxypropane-1-sulfonate (DHPS). This compound has no currently recognized role in the marine microbial food web. As the genes for DHPS catabolism have limited distribution among bacterial taxa, T. pseudonana may use this sulfonate for targeted feeding of beneficial associates. Indeed, DHPS was both a major component of the T. pseudonana cytosol and an abundant microbial metabolite in a diatom bloom in the eastern North Pacific Ocean. Moreover, transcript analysis of the North Pacific samples provided evidence of DHPS catabolism by Roseobacter populations. Other such biogeochemically important metabolites may be common in the ocean but difficult to discriminate against the complex chemical background of seawater. Bacterial transformation of this diatom-derived sulfonate represents a previously unidentified and likely sizeable link in both the marine carbon and sulfur cycles.

A typical marine bacterial cell in coastal seawater contains only B200 molecules of mRNA, each of which lasts only a few minutes before being degraded. Such a surprisingly small and dynamic cellular mRNA reservoir has important implications for understanding the bacterium's responses to environmental signals, as well as for our ability to measure those responses. In this perspective, we review the available data on transcript dynamics in environmental bacteria, and then consider the consequences of a small and transient mRNA inventory for functional metagenomic studies of microbial communities.

Significance The microbial community of the Amazon River Plume determines the fate of the world’s largest input of terrestrial carbon and nutrients to the ocean. By benchmarking with internal standards during sample collection, we determined that each liter of plume seawater contains 1 trillion genes and 50 billion transcripts from thousands of bacterial, archaeal, and eukaryotic taxa. Gene regulation by taxa inhabiting distinct microenvironments provides insights into micron-scale patterns of transformations in the marine carbon, nitrogen, phosphorus, and sulfur cycles in this globally important ecosystem.

BackgroundThe Amazon River is by far the world’s largest in terms of volume and area, generating a fluvial export that accounts for about a fifth of riverine input into the world’s oceans. Marine microbial communities of the Western Tropical North Atlantic Ocean are strongly affected by the terrestrial materials carried by the Amazon plume, including dissolved (DOC) and particulate organic carbon (POC) and inorganic nutrients, with impacts on primary productivity and carbon sequestration.ResultsWe inventoried genes and transcripts at six stations in the Amazon River plume during June 2010. At each station, internal standard-spiked metagenomes, non-selective metatranscriptomes, and poly(A)-selective metatranscriptomes were obtained in duplicate for two discrete size fractions (0.2 to 2.0 μm and 2.0 to 156 μm) using 150 × 150 paired-end Illumina sequencing. Following quality control, the dataset contained 360 million reads of approximately 200 bp average size from Bacteria, Archaea, Eukarya, and viruses. Bacterial metagenomes and metatranscriptomes were dominated by Synechococcus, Prochlorococcus, SAR11, SAR116, and SAR86, with high contributions from SAR324 and Verrucomicrobia at some stations. Diatoms, green picophytoplankton, dinoflagellates, haptophytes, and copepods dominated the eukaryotic genes and transcripts. Gene expression ratios differed by station, size fraction, and microbial group, with transcription levels varying over three orders of magnitude across taxa and environments.ConclusionsThis first comprehensive inventory of microbial genes and transcripts, benchmarked with internal standards for full quantitation, is generating novel insights into biogeochemical processes of the Amazon plume and improving prediction of climate change impacts on the marine biosphere.

The trophic linkage between marine bacteria and phytoplankton in the surface ocean is a key step in the global carbon cycle, with almost half of marine primary production transformed by heterotrophic bacterioplankton within hours to weeks of fixation. Early studies conceptualized this link as the passive addition and removal of organic compounds from a shared seawater reservoir. Here, we analysed transcript and intracellular metabolite patterns in a two-member model system and found that the presence of a heterotrophic bacterium induced a potential recognition cascade in a marine phytoplankton species that parallels better-understood vascular plant response systems. Bacterium Ruegeria pomeroyi DSS-3 triggered differential expression of >80 genes in diatom Thalassiosira pseudonana CCMP1335 that are homologs to those used by plants to recognize external stimuli, including proteins putatively involved in leucine-rich repeat recognition activity, second messenger production and protein kinase cascades. Co-cultured diatoms also downregulated lipid biosynthesis genes and upregulated chitin metabolism genes. From differential expression of bacterial transporter systems, we hypothesize that nine diatom metabolites supported the majority of bacterial growth, among them sulfonates, sugar derivatives and organic nitrogen compounds. Similar recognition responses and metabolic linkages as observed in this model system may influence carbon transformations by ocean plankton.