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. 2015 Jan 13;112(2):453-7.
doi: 10.1073/pnas.1413137112. Epub 2014 Dec 29.

Cryptic Carbon and Sulfur Cycling Between Surface Ocean Plankton

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Free PMC article

Cryptic Carbon and Sulfur Cycling Between Surface Ocean Plankton

Bryndan P Durham et al. Proc Natl Acad Sci U S A. .
Free PMC article

Abstract

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 B12 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.

Keywords: DHPS; bacteria; diatoms; sulfonates; vitamin B12.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
Recovery of Thalassiosira pseudonana growth by addition of exogenous B12 (filled circles) or Ruegeria pomeroyi DSS-3 (open circles) compared with the B12-limited control (filled triangles). The star indicates the growth stage at which diatom cells were collected for RNA and metabolite analyses. (Inset) Cell counts for T. pseudonana following addition of exogenous B12 (filled circles) or R. pomeroyi (open circles) and for cogrown (open squares) or control (filled squares) R. pomeroyi over the first 2 d of the experiment. Error bars represent the SD of duplicate cultures.
Fig. 2.
Fig. 2.
DHPS transport and degradation genes in marine roseobacter R. pomeroyi DSS-3 (blue font) that were up-regulated (purple boxes, fold-change up-regulation indicated underneath) during cogrowth with T. pseudonana. Genes mediating metabolism of sulfopyruvate to cysteate (coa and gdh) were not differentially expressed, consistent with previous work (32). Two alternate routes of DHPS degradation present in members of the Roseobacter clade are shown in gray (Table S3). Bold arrows indicate transporters. Inset: RT-qPCR quantification of hpsN transcripts in R. pomeroyi in coculture with T. pseudonana (Thps; see Fig. 1, open circles) and in sterile f/2 seawater medium (SW) after 8 h, and during exponential growth with acetate or DHPS as the sole carbon source. Error bars represent SD of three technical replicates from duplicate cultures.
Fig. 3.
Fig. 3.
A Bayesian phylogenetic tree derived from reference HpsN sequences including experimentally verified sequences (bold) and orthologs in marine genomes available through the Integrated Microbial Genomes database (img.jgi.doe.gov; see Table S3 for additional information). The tree was constructed using the P4 software following a χ2 test on posterior distributed samples showing that a Bayesian composition-homogeneous model was adequate. Outgroups included a variety of histidinol dehydrogenase sequences. The value near each internal branch is the posterior probability, and the scale bar indicates the number of substitutions per site. Alphaproteobacterial HpsN clade sequences (and one gammaproteobacterial sequence from strain HIMB30) are marked with a bar, the clade containing Roseobacter sequences is highlighted by the purple box, and the R. pomeroyi DSS-3 sequence is marked by a star. HpsN paralogs in Roseobacter genomes for which function has not been determined are marked with a dashed bar. The remaining sequences are candidate HpsN proteins with varying levels of bioinformatic support. Locus tags are given in parentheses. Tree topologies based on alternate tree-building algorithms are given in Fig. S3.
Fig. 4.
Fig. 4.
Concentrations of selected metabolites in the T. pseudonana cytosol during exponential growth in B12-replete medium (+B12), in coculture with R. pomeroyi DSS-3 (+DSS-3), and in B12-limited medium (−B12), as analyzed by ultra-performance liquid chromatography mass spectrometry. Error bars represent SD of duplicate cultures.
Fig. 5.
Fig. 5.
DHPS cycling in the eastern North Pacific Ocean. (A) Chlorophyll a concentrations, diatom counts, and Roseobacter-clade hpsN transcript abundance at four stations along the Line P transect. (B) Total ion current chromatogram for the Station P4 sample collected by triple-stage quadrupole mass spectrometry, with insets showing DHPS and DMSP peak details. R2 values of standard curves with authentic standards were 0.98 for both compounds. Other identified compounds include glycine betaine (1.66 min; coeluting with additional small organic acids), phenylalanine (3.63 min), a mixture of thymidine and 5-methylthioadenosine (6.49 min), and the deuterated biotin injection standard (9.36 min; coeluting with lesser amounts of riboflavin and biotin). (C) DHPS and DMSP concentrations as a percent (by mass) of 30 measured metabolites in the eukaryotic plankton size fraction (>1.6 μm diameter) at four Line P stations.

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