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Methane Production by Phosphate-Starved SAR11 Chemoheterotrophic Marine Bacteria

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Methane Production by Phosphate-Starved SAR11 Chemoheterotrophic Marine Bacteria ARTICLE Received 9 Feb 2014 | Accepted 9 Jun 2014 | Published 7 Jul 2014 DOI: 10.1038/ncomms5346 Methane production by phosphate-starved SAR11 chemoheterotrophic marine bacteria Paul Carini1,*,w, Angelicque E. White2,*, Emily O. Campbell1 & Stephen J. Giovannoni1 The oxygenated surface waters of the world’s oceans are supersaturated with methane relative to the atmosphere, a phenomenon termed the ‘marine methane paradox’. The production of methylphosphonic acid (MPn) by marine archaea related to Nitrosopumilus maritimus and subsequent decomposition of MPn by phosphate-starved bacterioplankton may partially explain the excess methane in surface waters. Here we show that Pelagibacterales sp. strain HTCC7211, an isolate of the SAR11 clade of marine a-proteobacteria, produces methane from MPn, stoichiometric to phosphorus consumption, when starved for phosphate. Gene transcripts encoding phosphonate transport and hydrolysis proteins are upregulated under phosphate limitation, suggesting a genetic basis for the methanogenic phenotype. Strain HTCC7211 can also use 2-aminoethylphosphonate and assorted phosphate esters for phosphorus nutrition. Despite strain-specific differences in phosphorus utilization, these findings identify Pelagibacterales bacteria as a source of biogenic methane and further implicate phosphate starvation of chemoheterotrophic bacteria in the long-observed methane supersaturation in oxygenated waters. 1 Department of Microbiology, Oregon State University, Corvallis, Oregon 97331, USA. 2 College of Earth, Ocean, and Atmospheric Sciences, Oregon State University, Corvallis, Oregon 97331, USA. * These authors contributed equally to this work. w Present address: University of Maryland Center for Environmental Sciences, Horn Point Laboratory, Cambridge, MD 21613, USA. Correspondence and requests for materials should be addressed to S.J.G. (email: [email protected]). NATURE COMMUNICATIONS | 5:4346 | DOI: 10.1038/ncomms5346 | www.nature.com/naturecommunications 1 & 2014 Macmillan Publishers Limited. All rights reserved. ARTICLE NATURE COMMUNICATIONS | DOI: 10.1038/ncomms5346 he simplest of all hydrocarbons, methane (CH4), is a potent observations of CH4 maxima below the surface mixed layer and 6 greenhouse gas that has 420-fold more warming potential the lack of diurnal variation of these CH4 levels point to Tthan carbon dioxide, making an understanding of its heterotrophic organisms as probable contributors to CH4 sources and sinks important for global climate models (reviewed production—provided a steady source of MPn is available and in Valentine1). Canonical microbial methanogenesis pathways that environmental conditions favour the utilization of dissolved operate under strictly anaerobic conditions2, such that organic phosphorus (DOP). Consistent with the hypothesis that methanogenesis is not favoured in marine surface waters where P-starved heterotrophic bacteria produce CH4, members of oxygen is abundant. Historically, the only known sites of classical marine Vibrionales and Rhodobacterales expressed C–P lyase methanogenesis in the surface ocean were the anaerobic genes in P-limited mesocosm studies that, when amended with microenvironments of faecal matter and the guts of certain fish MPn, also generated CH4 (ref. 17). 3,4 or plankton . Yet, CH4 profiles in the open ocean show The SAR11 clade of oligotrophic a-proteobacteria (Pelagibac- subsurface maxima associated with the pycnocline (density, terales) are the numerically dominant chemoheterotrophic cells in 28 st ¼ 25.2–25.9; 50–200 m) where CH4 is generally marine euphotic zones worldwide . Environmental and supersaturated in relationship to atmospheric equilibrium5,6. laboratory studies have elucidated the forms of dissolved How this methane comes to be produced in oxygenic water organic matter Pelagibacterales bacteria use, including reduced masses is the basis of a phenomenon coined the ‘oceanic methane sulphur compounds, amino acids, one-carbon compounds, paradox’7, which is particularly intriguing given that the isotopic organic acids (reviewed in Tripp29) and vitamin precursors30. composition of subsurface CH4 maxima is inconsistent with that Despite a high degree of genomic conservation between of anaerobic microenvironments8. Pelagibacterales genomes31, strategies for acquiring P appear to An alternate hypothesis has been proposed: CH4 is produced vary between Pelagibacterales isolates. For example, compared when marine microorganisms use methylphosphonic acid (MPn) with the northeast Pacific Ocean isolate, ‘Candidatus Pelagibacter as a resource for phosphorus (P)9. Several lines of evidence ubique’ strain HTCC1062 (str. HTCC1062, herein), the genome support this ‘aerobic methane production’ hypothesis: (i) the C–P of Pelagibacterales sp. strain HTCC7211 (str. HTCC7211), 32 lyase enzyme complex catabolizes MPn to CH4, releasing isolated from the North Atlantic Ocean in the Sargasso Sea , 10,11 phosphate (Pi) that can be used for growth (reviewed in encodes for additional proteins involved in organophosphorus 12 20 White and Metcalf ); (ii) C–P lyase gene sequences are present transport (PhnCDEE2) and phosphonate utilization (sometimes abundant) in marine environments13–17; (iii) natural (PhnGHIJKLNM), suggesting that the two organisms have 9,17 seawater samples incubated with MPn release CH4 ; (iv) evolved different adaptive strategies for P acquisition related to biosynthesis of MPn by Nitrosopumilus maritimus SCM1, a niche partitioning14. member of the ubiquitous and abundant Marine Group I (MGI) Here, building on these genomic insights we test the hypothesis archaea was recently demonstrated18; and (v) ca. 0.6% of that Pelagibacterales chemoheterotrophic bacteria encoding the microbes in marine surface communities contain genes C–P lyase complex produce CH4 from MPn when Pi starved. We 18 encoding the MPn synthase . Taken together, these findings show that str. HTCC7211 produces CH4 from MPn in suggest the observed CH4 supersaturation can be explained by the proportions stoichiometric to P demand. Moreover, we present natural synthesis of MPn and subsequent hydrolysis for purposes rates of CH4 production under ideal growth conditions, together of P nutrition by marine plankton. with the genetic response to P starvation in the Pelagibacterales. For this process to act as a substantial source of CH4, there These data suggest Pelagibacterales are one of the leading must be an ecophysiological niche for MPn utilization in the contributors to CH4 dynamics in Pi-deficient oligotrophic gyres. oxygenic surface ocean. Isolated cultures of Escherichia coli, Pseudomonas spp. and other heterotrophic bacteria10,12, as well as marine autotrophs such as Trichodesmium19, have been shown to Results use MPn as a sole P source. In these organisms, MPn degradation The capacity of Pelagibacterales strains HTCC1062 and proceeds via the C–P lyase pathway and is induced by HTCC7211 to grow on multiple alternate P sources, including 12,20–23 Pi starvation . Building on these findings, studies phosphite, phosphonates and phosphate esters, was tested. Strain 9 17 by Karl et al. and Martı´nez et al. showed that when surface HTCC1062 grew on Pi and did not use added DOP (Fig. 1). In seawater is amended with glucose and a nitrogen source contrast, str. HTCC7211 used a broad range of alternate (to stimulate Pi-limiting conditions), MPn hydrolysis and CH4 compounds for P nutrition, including P esters (phosphoserine, production proceeds at rates that scale inversely with the glucose 6-phosphate and ribose 5-phosphate), phosphonates addition of exogenous Pi. The authors implicate a combination (2-aminoethylphosphonic acid and MPn) and reduced inorganic of heterotrophic marine bacteria, together with natural P (phosphite) (Fig. 1). In all cases, diauxic growth was observed assemblages of Trichodesmium spp., as drivers of this when str. HTCC7211 cells were grown with an alternate P source metabolism9,17. These findings are consistent with studies of (Fig. 2); this growth pattern is presumably related to a transition 23 24 gene expression and methane production in Trichodesmium from growth on Pi to growth on organic P resources as has been erythraeum IMS101 that show induction of C–P lyase genes described for other organisms33,34. There was no significant under P starvation and subsequent methane production from difference in negative control (no Pi added) cell yields and the cell MPn. yields attained when glucose 6-phosphate, ribose 5-phosphate, Although these experiments provide definitive evidence for MPn, 2-AEP and phosphoserine were supplied to str. HTCC1062 potential MPn utilization in the surface ocean, they do not (Fig. 1). We presume that this is an indication that abiotic Pi necessarily address the CH4 supersaturation observed at the release from these compounds is negligible. The increased str. pycnocline, nor the organism(s) responsible for production of HTCC1062 cell yields when grown with phosphite as a sole excess CH4 in these deep layers of the euphotic zone. It seems source of P could result from (i) trace amounts of phosphate; (ii) unlikely that the activity of large buoyant genera such as abiotic conversion (oxidation) of phosphite to phosphate; or (iii) Trichodesmium can wholly explain the subsurface CH4 features the ability of str. HTCC1062 to enzymatically oxidize phosphite given that Trichodesmium are largely observed within or at the to phosphate via an unknown mechanism. At this time we do not 25,26 base of surface mixed layer and that CH4 supersaturation
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