Dataset Information

Sulfolipids dramatically decrease phosphorus demand by picocyanobacteria in oligotrophic marine environments.

ABSTRACT: There is growing evidence that dissolved phosphorus can regulate planktonic production in the oceans' subtropical gyres, yet there is little quantitative information about the biochemical fate of phosphorus in planktonic communities. We observed in the North Pacific Subtropical Gyre (NPSG) that the synthesis of membrane lipids accounted for 18-28% of the phosphate (PO4(3-)) taken up by the total planktonic community. Paradoxically, Prochlorococcus, the cyanobacterium that dominates NPSG phytoplankton, primarily synthesizes sulfoquinovosyldiacylglycerol (SQDG), a lipid that contains sulfur and sugar instead of phosphate. In axenic cultures of Prochlorococcus, it was observed that <1% of the total PO4(3-) uptake was incorporated into membrane lipids. Liquid chromatography/mass spectrometry of planktonic lipids in the NPSG confirmed that SQDG was the dominant membrane lipid. Furthermore, the analyses of SQDG synthesis genes from the Sargasso Sea environmental genome showed that the use of sulfolipids in subtropical gyres was confined primarily to picocyanobacteria; no sequences related to known heterotrophic bacterial SQDG lineages were found. This biochemical adaptation by Prochlorococcus must be a significant benefit to these organisms, which compete against phospholipid-rich heterotrophic bacteria for PO4(3-). Thus, evolution of this "sulfur-for-phosphorus" strategy set the stage for the success of picocyanobacteria in oligotrophic environments and may have been a major event in Earth's early history when the relative availability of sulfate and PO4(3-) were significantly different from today's ocean.

SUBMITTER: Van Mooy BA

PROVIDER: S-EPMC1482627 | biostudies-literature | 2006 Jun

REPOSITORIES: biostudies-literature

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Sulfolipids dramatically decrease phosphorus demand by picocyanobacteria in oligotrophic marine environments.

Van Mooy Benjamin A S BA Rocap Gabrielle G Fredricks Helen F HF Evans Colleen T CT Devol Allan H AH

Proceedings of the National Academy of Sciences of the United States of America 20060526 23

There is growing evidence that dissolved phosphorus can regulate planktonic production in the oceans' subtropical gyres, yet there is little quantitative information about the biochemical fate of phosphorus in planktonic communities. We observed in the North Pacific Subtropical Gyre (NPSG) that the synthesis of membrane lipids accounted for 18-28% of the phosphate (PO4(3-)) taken up by the total planktonic community. Paradoxically, Prochlorococcus, the cyanobacterium that dominates NPSG phytopla ...[more]

PMID: 16731626

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Project description:Large swaths of the nutrient-poor surface ocean are dominated numerically by cyanobacteria (Prochlorococcus), cyanobacterial viruses (cyanophage), and alphaproteobacteria (SAR11). How these groups thrive in the diverse physicochemical environments of different oceanic regions remains poorly understood. Comparative metagenomics can reveal adaptive responses linked to ecosystem-specific selective pressures. The Red Sea is well-suited for studying adaptation of pelagic-microbes, with salinities, temperatures, and light levels at the extreme end for the surface ocean, and low nutrient concentrations, yet no metagenomic studies have been done there. The Red Sea (high salinity, high light, low N and P) compares favorably with the Mediterranean Sea (high salinity, low P), Sargasso Sea (low P), and North Pacific Subtropical Gyre (high light, low N). We quantified the relative abundance of genetic functions among Prochlorococcus, cyanophage, and SAR11 from these four regions. Gene frequencies indicate selection for phosphorus acquisition (Mediterranean/Sargasso), DNA repair and high-light responses (Red Sea/Pacific Prochlorococcus), and osmolyte C1 oxidation (Red Sea/Mediterranean SAR11). The unexpected connection between salinity-dependent osmolyte production and SAR11 C1 metabolism represents a potentially major coevolutionary adaptation and biogeochemical flux. Among Prochlorococcus and cyanophage, genes enriched in specific environments had ecotype distributions similar to nonenriched genes, suggesting that inter-ecotype gene transfer is not a major source of environment-specific adaptation. Clustering of metagenomes using gene frequencies shows similarities in populations (Red Sea with Pacific, Mediterranean with Sargasso) that belie their geographic distances. Taken together, the genetic functions enriched in specific environments indicate competitive strategies for maintaining carrying capacity in the face of physical stressors and low nutrient availability.

Project description:Picocyanobacteria Prochlorococcus and Synechococcus are abundant in the global oceans and subject to active viral infection. In this study, the genetic diversity of picocyanobacteria and the genetic diversity of cyanopodoviruses were synchronously investigated along water columns in the equatorial Indian Ocean and over a seasonal time course in the coastal Sanya Bay, South China Sea. Using the 16S-23S rRNA internal transcribed spacer (ITS)-based clone library and quantitative PCR (qPCR) analyses, the picocyanobacterial community composition and abundance were determined. Sanya Bay was dominated by clade II Synechococcus during all the seasons, and a typical population shift from high-light-adapted Prochlorococcus to low-light-adapted Prochlorococcus was found along the vertical profiles. Strikingly, the DNA polymerase gene sequences of cyanopodoviruses revealed a much greater genetic diversity than we expected. Nearly one-third of the phylogenetic groups were newly described here. No apparent seasonal pattern was observed for the Sanya Bay picocyanobacterial or cyanopodoviral communities. Different dominant cyanopodovirus lineages were identified for the coastal area, upper euphotic zone, and middle-to-lower euphotic zone of the open ocean. Diversity indices of both picocyanobacteria and cyanopodoviruses were highest in the middle euphotic zone and both were lower in the upper euphotic zone, reflecting a host-virus interaction. Cyanopodoviral communities differed significantly between the upper euphotic zone and the middle-to-lower euphotic zone, showing a vertical pattern similar to that of picocyanobacteria. However, in the surface waters of the open ocean, cyanopodoviruses exhibited no apparent biogeographic pattern, differing from picocyanobacteria. This study demonstrates correlated distribution patterns of picocyanobacteria and cyanopodoviruses, as well as the complex biogeography of cyanopodoviruses.IMPORTANCE Picocyanobacteria are highly diverse and abundant in the ocean and display remarkable global biogeography and a vertical distribution pattern. However, how the diversity and distribution of picocyanobacteria affect those of the viruses that infect them remains largely unknown. Here we synchronously analyzed the community structures of cyanopodoviruses and picocyanobacteria at spatial and temporal scales. Both spatial and temporal variations of cyanopodoviral communities can be linked to those of picocyanobacteria. The coastal area, upper euphotic zone, and middle-to-lower euphotic zone of the open ocean have distinct cyanopodoviral communities, showing horizontal and vertical variation patterns closely related to those of picocyanobacteria. These findings emphasize the driving force of host community in shaping the biogeographic structure of viruses. Our work provides important information for future assessments of the ecological roles of viruses and hosts for each other.

Dataset Information

Sulfolipids dramatically decrease phosphorus demand by picocyanobacteria in oligotrophic marine environments.

Publications

Sulfolipids dramatically decrease phosphorus demand by picocyanobacteria in oligotrophic marine environments.

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