Anomalous Δ13c in Particulate Organic Carbon at the Chemoautotrophy Maximum in the 1
Total Page：16
File Type：pdf, Size：1020Kb
13 RESEARCH ARTICLE Anomalous δ C in Particulate Organic Carbon at the 10.1029/2019JG005276 Chemoautotrophy Maximum in the Cariaco Basin Special Section: Mary I. Scranton1 , Gordon T. Taylor1 , Robert C. Thunell2,3 , Frank E. Muller‐Karger4, Special Collection to Honor 4,5 6 7 7 the Career of Robert C. Yrene Astor , Peter Swart , Virginia P. Edgcomb , and Maria G. Pachiadaki Thunell 1School of Marine and Atmospheric Sciences, Stony Brook University, Stony Brook, USA, 2Department of Geological Sciences, University of South Carolina, Columbia, SC, USA, 3Deceased on 30 July 2018, 4College of Marine Science, Key Points: University of South Florida, St. Petersburg, FL, USA, 5Fundación La Salle de Ciencias Naturales, EDIMAR, Caracas, • Particulate organic carbon at the O2/ Venezuela, 6Rosenstiel School of Marine and Atmospheric Science, University of Miami, Miami, FL, USA, 7Woods Hole H S interface in the Cariaco is 2 Oceanographic Institution, Woods Hole, MA, USA occasionally isotopically very heavy 13 (δ CPOC as high as −16‰) 13 • The maximum in δ CPOC corresponds with low C/N ratios of Abstract A chemoautotrophy maximum is present in many anoxic basins at the sulfidic layer's upper particulate organic matter, implying boundary, but the factors controlling this feature are poorly understood. In 13 of 31 cruises to the Cariaco the carbon is relatively fresh Basin, particulate organic carbon (POC) was enriched in 13C(δ13C as high as −16‰) within the • The maximum also corresponds POC with peaks in chemoautotrophy and oxic/sulfidic transition compared to photic zone values (−23 to −26‰). During “heavy” cruises, fluxes of O2 − − RuBisCO form II genes implying and [NO3 +NO2 ] to the oxic/sulfidic interface were significantly lower than during “light” cruises. δ13 that CPOC is affected by Cruises with isotopically heavy POC were more common between 2013 and 2015 when suspended particles chemoautotrophy below the photic zone tended to be nitrogen rich compared to later cruises. Within the chemoautotrophic 13 Supporting Information: layer, nitrogen‐rich particles (molar ratio C/N< 10) were more likely to be C‐enriched than nitrogen‐poor • Supporting Information S1 particles, implying that these inventories were dominated by living cells and fresh detritus rather than • Supporting Information S2 laterally transported or extensively decomposed detritus. During heavy cruises, 13C enrichments persisted to 1,300 m, providing the first evidence of downward transport of chemoautotrophically produced POC. Dissolved inorganic carbon assimilation during heavy cruises (n = 3) was faster and occurred deeper than Correspondence to: M. I. Scranton, during light cruises (n = 2). Metagenomics data from the chemoautotrophic layer during two cruises [email protected] support prevalence of microorganisms carrying RuBisCO form II genes, which encode a carbon fixation enzyme that discriminates less against heavy isotopes than most other carbon fixation enzymes, and Citation: metatranscriptomics data indicate that higher expression of form II RuBisCO genes during the heavy cruises Scranton, M. I., Taylor, G. T., Thunell, at depths where essential reactants coexist are responsible for the isotopically heavier POC. R. C., Muller‐Karger, F. E., Astor, Y., Swart, P., et al. (2020). Anomalous δ13C in particulate organic carbon at the chemoautotrophy maximum in the 1. Introduction Cariaco Basin. Journal of Geophysical Research: Biogeosciences, 125, Carbon isotopic composition of particulate organic matter in aquatic environments is initially determined by e2019JG005276. https://doi.org/ the isotopic composition of the dissolved inorganic carbon (δ13C ) used by autotrophs and by the isotopic 10.1029/2019JG005276 DIC 13 fractionation that takes place when carbon is fixed. DIC in seawater typically has a δ CDIC of around 0 to 13 Received 10 JUN 2019 −1‰ (Hoefs, 2009) and δ CPOC of marine particulate organic matter typically varies between −18 and Accepted 3 JAN 2020 −34‰, depending on location (Goericke & Fry, 1994). While important exceptions exist (see Fry & Accepted article online 30 JAN 2020 Wainright, 1991; Reinfelder et al., 2000), most phytoplankton appear to use the C3 carbon fixation pathway leading to overall isotopic fractionation factors (εp) of 16 to 25, which result in phytoplankton biomass with δ13C signatures of −19 to −24‰. (Fry, 2006; O'Leary, 1988). 13 One might expect to see declines in δ CPOC at depths where chemoautotrophs fix carbon in stratified mar- ine systems, such as observed in Kyllaren fjord (van Breugel et al., 2005). This results from isotopically light organic matter being preferentially respired back to DIC pool throughout the water column. Thus, DIC and 13 δ CPOC produced by chemoautotrophs would become lighter at depths where significant respiration is occurring. However, the extent of isotopic fractionation by chemoautotrophic microorganisms varies among taxa. For example, ε‐proteobacterial symbionts of hydrothermal vent gastropods and polychaetes, which chemoautotrophically fixCO2 by the reductive tricarboxylic acid (rTCA) cycle, can be isotopically much hea- δ13 − − ‰ vier ( CBIOMASS = 8to 12 ) than typical photoautotrophic primary producers (Campbell et al., 2003; Zbinden et al., 2015). In fact, at least six different CO2 fixation pathways are known and have widely varying ©2020. American Geophysical Union. energetic costs (ATP and reductants consumed per pyruvate molecule produced) and carbon isotopic fractio- δ13 − − ‰ All Rights Reserved. nations yielding CBIOMASS ranging from 0.2 to 30 (reviewed in Berg et al., 2010, and Hügler & Sievert, SCRANTON ET AL. 1of17 Journal of Geophysical Research: Biogeosciences 10.1029/2019JG005276 2011). Even among organisms that share the Calvin‐Benson‐Basham (CBB) reductive pentose phosphate cycle, εp varies depending on which form of the ribulose‐1,5‐bisphosphate carboxylase/oxygenase (RuBisCO) enzyme is used. For example, Robinson and Cavanaugh (1995) determined that endosymbiotic γ‐proteobacteria in the hydrothermal vent vestimintiferan Riftia patchyptila fix carbon with form II δ13 − − ‰ − − ‰ RuBisCO and produce CBIOMASS of 9to 16 compared to 17 to 25 evident in organisms using δ13 form I RuBisCO. Thus, CBIOMASS signatures can provide insights into mechanisms by which DIC is assimilated autotrophically. The widespread importance of chemoautotrophy in environmental redox gradients has become increas- ingly evident in recent years. Significant dark carbon fixation has been reported in the Black Sea (Jørgensen et al., 1991; Yilmaz et al., 2006), in the Cariaco Basin (Taylor et al., 2001; Tuttle & Jannasch, 1973), in the Baltic Sea (Jost et al., 2008), in Mariager fjord (Zopfi et al., 2001), in Namibian shelf waters (Lavik et al., 2009), and in the oxygen minimum zones of the Eastern Tropical South Pacific (Schunck et al., 2013). In most cases, a light scattering (particulate) maximum coincides with elevated microbial bio- mass in the upper portion of the sulfidic zone (Taylor et al., 2001; Yilmaz et al., 2006) where sulfur‐ oxidizing bacteria have been identified (Glaubitz et al., 2010; Jørgensen et al., 1991; Kirkpatrick et al., 2018; Tuttle & Jannasch, 1972; Zopfi et al., 2001). Modeling geochemical balances that are consistent with measured rates of dark carbon fixation has been challenging (Li et al., 2012). However, recent biogeochem- ical flux models yield much better agreement between supply and demand for reactants (Louca, Scranton, et al., 2019, Louca, Astor, et al., 2019). As in many other stratified oxygen‐depleted water columns, chemoautotrophic assemblages across the Cariaco's redox transitional zone are comprised of ammonia‐oxidizing, nitrite‐oxidizing, anaerobic ammonia‐oxidizing (anammox), and reduced sulfur‐oxidizing microorganisms (Cernadas‐Martin et al., 2017; Montes et al., 2013; Suter et al., 2018; Taylor et al., 2001; Wakeham et al., 2012). During the present study's timeframe (2013–2017), ammonia‐oxidizing archaea in marine group I, ammonia‐oxidizing beta‐ and γ‐proteobacteria, and nitrite‐oxidizing Nitrospina (δ‐proteobacteria) have been observed across the oxycline (Cernadas‐Martin et al., 2017; Suter et al., 2018). Peaks in anammox bacteria (Candidatus Scalindua) also have been detected in Cariaco's transitional waters by an array of methods, including lipid biomarkers, fluorescence in situ hybridization, quantitative polymerase chain reaction (PCR), and 16S rRNA sequencing (Wakeham et al., 2012; Rodriguez et al., 2015; Cernadas‐Martin et al., 2017; Suter et al., 2018). Over the entire Cariaco Ocean Time‐Series program (1995–2017), taxa comprising some chemoautotrophic functional groups have changed demonstrably. For example, the dominant S‐oxidizers taxa early in the record were ε‐proteobacteria, which appear to have been replaced by members of the γ‐proteobacteria after May 2009 (Lin et al., 2006; Madrid et al., 2001; Taylor et al., 2018). Putative γ‐proteobacteria S‐oxidizers (GSO) dominating the shallow anoxic and euxinic depths were represented by the SUP05 clade and a single OTU in the Ectothiorhodospiraceae family, closely matching an uncultured Thiorhodospira sp. (Suter et al., 2018). Related GSOs dominate redoxclines of other oxygen‐depleted environments, such as the Black Sea (Fuchsman et al., 2011), Baltic Sea (Glaubitz et al., 2013), shelf water on the Namibian coast (Lavik et al., 2009), Saanich Inlet (Walsh et al., 2009), and the Pacific Ocean OMZs (Stewart et al., 2012). Other likely che- moautotrophic sulfur oxidizers were also present in Cariaco surveys, including