A Parasitic Arsenic Cycle That Shuttles Energy from Phytoplankton to Heterotrophic Bacterioplankton

Abstract

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.

SAR11 bacteria have a high affinity and multifunctional glycine betaine transporter

“…Our research strategy is to explore ecologically relevant metabolic processes with genomes, cell cultures and field experiments (Sun et al, 2011;Halsey et al, 2017;Giovannoni et al, 2019). This approach addresses properties of cells that are not predictable from omics data but contribute to activities observed at the ecosystem level.…”

Unlocking the genomic taxonomy of theProchlorococcuscollective

“…Ecological transitions and changes in the oceans trigger natural genetic engineering and genome changes on a massive scale [25,143]. The PC has evolved in multiple ecologic niches in the global ocean and participates in relevant biogeochemical cycles, such as the recently postulated parasitic arsenic cycle between Eurycolium and Pelagibacter ubique [144,145]. We demonstrated here that the current PC is a diverse group of genera that are clearly distinguishable by eco-genomics.…”

Pelagibacter metabolism of diatom‐derived volatile organic compounds imposes an energetic tax on photosynthetic carbon fixation

“…The volatile components of DOC produced by T. pseudonana were demonstrated to be sources of energy for HTCC1062, as some of the identified VOCs stimulated ATP production by the bacteria, but their contribution to the observed growth enhancement of HTCC1062 in co‐culture remains uncertain, with the exception of acetaldehyde ( m / z 45.033), which can be incorporated into HTCC1062 biomass (Halsey et al ., ). Experiments examining the metabolism of VOCs by HTCC1062 in greater detail are necessary to understand their importance as substrates, but studies on the metabolism of other carbon substrates by the SAR11 clade indicate that many organic compounds are oxidized for energy, rather than used for growth (Sun et al ., ; Halsey et al ., ; Giovannoni et al ., ).…”

“…As a result of genomic streamlining, Pelagibacter have specific carbon and nutrient requirements (Tripp et al ., ; Carini et al ., ) and have evolved to transport and metabolize a variety of phytoplankton‐derived low‐molecular‐weight carbon compounds, including VOCs, using a limited genetic repertoire (Giovannoni et al ., ). For example, Pelagibacter metabolize a variety of methylated and volatile compounds, including methanol, dimethylsulfide (DMS), formaldehyde, acetaldehyde, methylamine and methylated arsenic species (Sun et al ., , ; Halsey et al ., ; Giovannoni et al ., ).…”