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Cyanobacteria and Cyanophage Contributions to Carbon and Nitrogen Cycling in an Oligotrophic Oxygen-Deficient Zone

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Cyanobacteria and Cyanophage Contributions to Carbon and Nitrogen Cycling in an Oligotrophic Oxygen-Deficient Zone The ISME Journal https://doi.org/10.1038/s41396-019-0452-6 ARTICLE Cyanobacteria and cyanophage contributions to carbon and nitrogen cycling in an oligotrophic oxygen-deficient zone 1,2 1,3 4,5 1 1,6 Clara A. Fuchsman ● Hilary I. Palevsky ● Brittany Widner ● Megan Duffy ● Michael C. G. Carlson ● 1 4 1 1 1 Jacquelyn A. Neibauer ● Margaret R. Mulholland ● Richard G. Keil ● Allan H. Devol ● Gabrielle Rocap Received: 21 June 2018 / Revised: 20 April 2019 / Accepted: 26 May 2019 © The Author(s) 2019. This article is published with open access Abstract Up to half of marine N losses occur in oxygen-deficient zones (ODZs). Organic matter flux from productive surface waters is considered a primary control on N2 production. Here we investigate the offshore Eastern Tropical North Pacific (ETNP) where a secondary chlorophyll a maximum resides within the ODZ. Rates of primary production and carbon export from the mixed layer and productivity in the primary chlorophyll a maximum were consistent with oligotrophic waters. However, sediment trap carbon and nitrogen fluxes increased between 105 and 150 m, indicating organic matter production within the ODZ. Metagenomic and metaproteomic characterization indicated that the secondary chlorophyll a maximum was Prochlorococcus fi 1234567890();,: 1234567890();,: attributable to the cyanobacterium , and numerous photosynthesis and carbon xation proteins were detected. The presence of chemoautotrophic ammonia-oxidizing archaea and the nitrite oxidizer Nitrospina and detection of nitrate oxidoreductase was consistent with cyanobacterial oxygen production within the ODZ. Cyanobacteria and cyanophage were also present on large (>30 μm) particles and in sediment trap material. Particle cyanophage-to-host ratio exceeded 50, suggesting that viruses help convert cyanobacteria into sinking organic matter. Nitrate reduction and anammox proteins were detected, congruent with previously reported N2 production. We suggest that autochthonous organic matter production within the ODZ contributes to N2 production in the offshore ETNP. Introduction fi Supplementary information The online version of this article (https:// The oxygen content of the Paci c Ocean has been doi.org/10.1038/s41396-019-0452-6) contains supplementary decreasing since the 1980s in response to increased oxygen material, which is available to authorized users. utilization [1]. Model predictions suggest a 1% reduction in fi ’ fi * the Paci c sO2 inventory will double the size of the Paci c Clara A. Fuchsman fi [email protected] oxygen-de cient zones (ODZs) [2]. Indeed, repeat mea- fi * Gabrielle Rocap surements indicate that the Eastern Tropical North Paci c [email protected] (ETNP) ODZ has thickened over the past 40 years and intruded into shallower waters [3]. In the absence of oxygen 1 School of Oceanography, University of Washington, Seattle, WA, as an electron acceptor, oxidized nitrogen species can be USA reduced to N2 via two main pathways: heterotrophic deni- fi 2 Horn Point Laboratory, University of Maryland, Cambridge, MD, tri cation and autotrophic anaerobic ammonia oxidation USA (anammox) [4, 5]. Both processes depend on organic mat- fi 3 Geosciences Department, Wellesley College, Wellesley, MA, ter, directly in the case of denitri cation and indirectly in USA the case of anammox, which can use ammonium released 4 Marine Chemistry and Geochemistry, Woods Hole Oceanographic during organic matter degradation as its reductant [6]. Institution, Woods Hole, MA, USA Organic matter flux has been correlated with N2 production – 5 Department of Ocean, Earth and Atmospheric Sciences, Old in the environment [7 11], and indeed, the addition of Dominion University, Norfolk, VA, USA sterilized sediment trap material significantly increased both fi 6 Faculty of Biology, Technion—Israel Institute of Technology, denitri cation and anammox rates in all three marine ODZs: Haifa, Israel the Arabian Sea, the Eastern Tropical South Pacific (ETSP), C. A. Fuchsman et al. and the ETNP [5, 12]. Up to half of marine N losses from meter, a Seabird SBE 43 Dissolved Oxygen Sensor, a N2 production occur in marine ODZs [13], so an increase in WETLabs ECO Chlorophyll Fluorometer, and a Biospherical/ the volume of ODZs may lead to an increase in N loss and Licor PAR/Irradiance Sensor were attached to the CTD stronger N limitation on primary producers globally. rosette. Hydrographic and nutrient data from the cruise are Due to sluggish circulation [14], most of the volume of deposited at http://data.nodc.noaa.gov/accession/0109846. the ETNP ODZs is offshore, where productivity is 10× Three free-floating surface-tethered sediment net traps lower than in coastal regions [15]. In general, the phyto- [24] were deployed at station BB2 at 105, 150, and 750 m. plankton communities responsible for organic matter pro- Sediment trap carbon and nitrogen fluxes were measured as duction also differ between coastal and offshore regions, in Babbin et al [5]. Logistics precluded duplicate mea- with larger eukaryotic phytoplankton more abundant in surements of sediment trap-derived flux estimates. Carbon coastal regions while cyanobacteria are the dominant pri- flux from 105 m was previously published [5], but carbon mary producers offshore [15]. Given this combination of fluxes from 150 and 750 m and nitrogen fluxes have not low primary productivity rates and the lower export effi- been previously published. ciency of communities dominated by smaller-celled phy- toplankton [16], export fluxes are expected to be lower in Productivity measurements the offshore ETNP. However, in addition to production in 17 surface waters, populations of the cyanobacterium Pro- Samples for triple oxygen isotope ( Δ; TOI) and O2/Ar chlorococcus have been found at depth within all three dissolved gas analysis were collected in duplicate from the major ODZs [17, 18] at a secondary chlorophyll a max- surface mixed layer on a coastal to open ocean transect imum where the 1% of the deeply penetrating blue irra- (station locations shown in Fig. 1 and station information diance (490 nm) overlaps with the ODZ [19]. Genetic listed in Table S1) and analyzed following the laboratory evidence using the 16S–23S ribosomal RNA (rRNA) procedures described in Palevsky et al. [25]. Gross primary internal transcribed spacer (ITS) region suggests that this production (GPP) rates can be calculated from mixed layer population may be composed of novel lineages of Pro- TOI by leveraging the unique isotopic signature of chlorococcus that are closely related to cultured isolates of atmospheric-derived oxygen, which is depleted in 17Oas the low light IV (LLIV) ecotype [20]. At five stations in the compared to photosynthetically derived oxygen due to ETNP, primary production was measured at the Pro- mass-independent fractionation in a stratospheric photo- chlorococcus-dominated secondary chlorophyll a maximum chemical reaction. The TOI system is insensitive to mass- [21]. It has been suggested that in situ production in the dependent fractionation as respiration removes oxygen, ODZ could significantly increase the organic C supply to isolating the influence of photosynthesis from respiration N2-producing heterotrophs [21]. Here we show productivity and enabling calculation of mixed layer GPP by combining and export measurements along with metaproteomic and TOI measurements with air–sea gas exchange rates [26]. metagenomic analyses that strongly supports this hypoth- Net community production (NCP) rates, which represent esis. The pathway to deliver organic carbon fixed by Pro- organic carbon export from the mixed layer under steady- chlorococcus cells to heterotrophic denitrifiers has not been state conditions, can similarly be calculated by combining established in the ODZ. Viruses have been implicated in biological oxygen supersaturation determined from mea- organic matter cycling in the ocean [22], and abundance of sured O2/Ar with air–sea gas exchange rates. cyanobacterial viruses have been shown to strongly corre- Mixed layer GPP and NCP rates were calculated from late with organic matter flux in the oxic oligotrophic ocean estimated air–sea gas transfer velocity and measured TOIs [23]. From the abundance and composition of cyano- ([27]; Eq. 7) and O2/Ar ([28]; Eq. 3), respectively. These bacterial viruses on particles, we suggest a role for these equations assume steady-state conditions and negligible viruses in the conversion of cells into sinking organic matter influence of mixing and advection in the mixed layer dis- in the ODZ. solved gas budget, which model results show to be a rea- sonable approximation for the ETNP in April [29]. Daily wind speed data from National Oceanic and Atmospheric Methods Administration National Climatic Data Center’s multiple- satellite Blended Sea Winds product (https://www.ncdc. Sampling noaa.gov/oa/rsad/air-sea/seawinds.html)wereusedtocal- culate air–sea gas transfer velocity [30] with the Reuer Samples were collected in April 2012 aboard the R/V et al. [28] weighting scheme. Uncertainty in GPP and NCP Thompson during cruise TN278 using 10 L Niskin bottles rates were determined using a Monte Carlo approach (as in attached to a 24 bottle CTD (conductivity–temperature–depth) [25]). Mixed layer GPP rates were converted to rates rosette. A Seabird 911 Conductivity Temperature Density equivalent to incubation-based net primary production Cyanobacteria and cyanophage contributions to carbon and nitrogen cycling in an oligotrophic. A. −1 B. MODIS chlorophyll (μg L ), 6−13 April 2012 N Flux (μmol/m2-d) 28oN 20 (m) 0 204060 10 0 24oN 5 100 200 2 o 300 20 N 1 400 0.5 500 16oN 0.2 600 700 0.1 N flux o 12 N 800 C flux 900 o 0 0.2 0.4 0.6 0.8 8 N 0.02 C Flux (mmol/m2-d) 132oW 126oW 120oW 114oW 108oW 102oW C. NPP 35±4 35±5 22±4 31±4 31±4 24±3 15±2 26±4 67±11 % Export 7±5% 1±5% 13±7% 10±5% 7±5% 1±6% 8±10% 4±6% 24±3% Chl a [μg-L-1] St Fig. 1 a Map of 8-day averaged satellite chlorophyll over the time Atlas.
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