No abstract

Volatile organic compounds (VOCs) produced by phytoplankton are molecules with high vapor pressures that can diffuse across cell membranes into the environment, where they become public goods. VOCs likely comprise a significant component of the marine dissolved organic carbon (DOC) pool utilized by microorganisms, but they are often overlooked as growth substrates because their diffusivity imposes analytical challenges. The roles of VOCs in the growth of the photoautotrophic diatom Thalassiosira pseudonana and heterotrophic bacterium Pelagibacter sp. HTCC1062 (SAR11) were examined using co-cultures and proton-transfer reaction time-of-flight mass spectrometry. VOCs at 82 m/z values were produced in the cultures, and the concentrations of 9 of these m/z values changed in co-culture relative to the diatom monoculture. Several of the m/z values were putatively identified, and their metabolism by HTCC1062 was confirmed by measuring ATP production. Diatom carbon fixation rates in co-culture with HTCC1062 were 20.3% higher than the diatom monoculture. Removal of VOCs from the T. pseudonana monoculture using a hydrocarbon trap caused a similar increase in carbon fixation (18.1%). These results show that a wide range of VOCs are cycled in the environment, and the flux of VOCs from phytoplankton to bacterioplankton imposes a large and unexpected tax on phytoplankton photosynthesis.

In many regions of the world oceans, phytoplankton face the problem of discriminating between phosphate, an essential nutrient, and arsenate, a toxic analogue. Many phytoplankton, including the most abundant phytoplankton group known,Prochlorococcus, detoxify arsenate (AsV) by reduction to arsenite (AsIII), followed by methylation and excretion of the methylated arsenic products. We synthesized [14C]dimethyl arsenate (DMA) and used it to show that culturedPelagibacterstrain HTCC7211 (SAR11) cells oxidize the methyl group carbons of DMA, producing14CO2and ATP. We measured [14C]DMA oxidation rates in the P-depleted surface waters of the Sargasso Sea, a subtropical ocean gyre. [14C]DMA was oxidized to14CO2by Sargasso Sea plankton communities at a rate that would cause turnover of the estimated DMA standing stock every 8.1 days. SAR11 strain HTCC7211, which was isolated from the Sargasso Sea, has a pair of arsenate resistance genes and was resistant to arsenate, showing no growth inhibition at As/P ratios of >65:1. Across the global oceans, there was a strong inverse relationship between the frequency of the arsenate reductase (LMWPc_ArsC) inPelagibactergenomes and phosphate concentrations. We propose that the demethylation of methylated arsenic compounds byPelagibacterand possibly other bacterioplankton, coupled with arsenate resistance, results in the transfer of energy from phytoplankton to bacteria. We dub this a parasitic cycle because the release of arsenate byPelagibacterin principle creates a positive-feedback loop that forces phytoplankton to continually regenerate arsenate detoxification products, producing a flow of energy to P-limited ocean regions.IMPORTANCEIn vast, warm regions of the oceans, phytoplankton face the problem of arsenic poisoning. Arsenate is toxic because it is chemically similar to phosphate, a scarce nutrient that phytoplankton cells need for growth. Many phytoplankton, including the commonest phytoplankton type in warm oceans,Prochlorococcus, detoxify arsenate by adding methyl groups. Here we show that the most abundant non-photosynthetic plankton in the oceans, SAR11 bacteria, remove the methyl groups, releasing poisonous forms of arsenic back into the water. We postulate that the methylation and demethylation of arsenic compounds creates a cycle in which the phytoplankton can never get ahead and must continually transfer energy to the SAR11 bacteria. We dub this a parasitic process and suggest that it might help explain why SAR11 bacteria are so successful, surpassing all other plankton in their numbers. Field experiments were done in the Sargasso Sea, a subtropical ocean gyre that is sometimes called an ocean desert because, throughout much of the year, there is not enough phosphorous in the water to support large blooms of phytoplankton. Ocean deserts are expanding as the oceans absorb heat and grow warmer.

The reproductive strategy of diatoms includes asexual and sexual phases, but in many species, including the model centric diatom Thalassiosira pseudonana, sexual reproduction has never been observed. Furthermore, the environmental factors that trigger sexual reproduction in diatoms are not understood. Although genome sequences of a few diatoms are available, little is known about the molecular basis for sexual reproduction. Here we show that ammonium reliably induces the key sexual morphologies, including oogonia, auxospores, and spermatogonia, in two strains of T. pseudonana, T. weissflogii, and Cyclotella cryptica. RNA sequencing revealed 1,274 genes whose expression patterns changed when T. pseudonana was induced into sexual reproduction by ammonium. Some of the induced genes are linked to meiosis or encode flagellar structures of heterokont and cryptophyte algae. The identification of ammonium as an environmental trigger suggests an unexpected link between diatom bloom dynamics and strategies for enhancing population genetic diversity.

Plants and phytoplankton are natural sources of the volatile organic compounds (VOCs) acetone and isoprene, which are reactive and can alter atmospheric chemistry. In earlier research we reported that, when co-cultured with a diatom, the marine bacterium Pelagibacter (strain HTCC1062; 'SAR11 clade') reduced the concentration of compounds tentatively identified as acetone and isoprene. In this study, experiments with Pelagibacter monocultures confirmed that these cells are capable of metabolizing acetone and isoprene at rates similar to bacterial communities in seawater and high enough to consume substantial fractions of the total marine acetone and isoprene budgets if extrapolated to global SAR11 populations. Homologues of an acetone/ cyclohexanone monooxygenase were identified in the HTCC1062 genome and in the genomes of a wide variety of other abundant marine taxa, and were expressed at substantial levels (c. 10 À4 of transcripts) across TARA oceans metatranscriptomes from ocean surface samples. The HTCC1062 genome lacks the canonical isoprene degradation pathway, suggesting an unknown alternative biochemical pathway is used by these cells for isoprene uptake. Fosmidomycin, an inhibitor of bacterial isoprenoid biosynthesis, blocked HTCC1062 growth, but the cells were rescued when isoprene was added to the culture, indicating SAR11 cells may be capable of synthesizing isoprenoid compounds from exogenous isoprene.