Elsevier

Marine Chemistry

Volume 231, 20 April 2021, 103955
Marine Chemistry

Accumulation of DOC in the South Pacific Subtropical Gyre from a molecular perspective

https://doi.org/10.1016/j.marchem.2021.103955Get rights and content

Highlights

  • DOM concentration and composition were assessed in the South Pacific.

  • DOC accumulates in oligotrophic South Pacific Subtropical gyre.

  • DOM molecular composition reveals low N/C and imprint of photodegradation.

  • Solid-phase extracted DOM fraction suitable to trace DOM ageing across ocean basins.

Abstract

The subtropical South Pacific Gyre (SPG) encompasses the largest oligotrophic region of the global ocean. In these remote waters dissolved organic matter (DOM) accumulates in the surface waters, though constituting a potential source of nutrients and energy to sustain microbial life. On a zonal transect across the SPG, we quantified bulk dissolved organic carbon (DOC) and assessed the DOM composition via ultrahigh resolution mass spectrometry (UHR-MS) of solid-phase extracted DOC (SPE-DOC) to elucidate the molecular-level reasons behind the apparent recalcitrance of the DOM prevailing in the SPG. We included a comparison between two individual formula assignment approaches to UHR-MS data in absorption and magnitude mode which yielded consistent results.

DOC concentrations exceeding 100 μmol C L−1 in the warm and saline waters of the central gyre were higher than in the surface waters of the adjacent western South Pacific. Along the transect, concentrations of SPE-DOC were less variable than bulk DOC. Nevertheless, molecular-level investigation revealed that the composition of the DOM accumulated in the central SPG generally conformed to characteristics of surface ocean DOM, but all assessed properties were more pronounced. We found high abundances of potentially labile unsaturated aliphatic molecular formulas and a low calculated degradation index for the DOM of likely marine microbial origin. Markedly decreased molar N/C ratios in the central gyre indicated preferential microbial utilization of nitrogen-containing DOM. A distinct imprint of extensive photochemical reworking was manifested in the low aromaticity of the DOM in the photic layer. Over the whole water column, ageing of DOM was evident through the small, but significant contribution of SPE-DOC to apparent oxygen utilization as well as on molecular level. Our findings demonstrate that SPE-DOC captures carbon fractions relevant on timescales of seasons to timescales covering ocean circulation and biogeochemical processes in stable gyre systems are imprinted in the DOM molecular composition.

Introduction

Dissolved organic carbon (DOC) in the oceans comprises a mixture of organic molecules spanning a wide range of ages, origins and reactivities. Its distribution and composition are controlled by biological and hydrographic processes. Biological production is mostly limited to the sunlit surface waters, while subduction and deep convection processes control deep ocean DOC concentrations (Carlson and Ducklow, 1995; Hansell and Carlson, 1998; Romera-Castillo et al., 2016).

Highest fluxes and at the same time low concentrations of freshly produced, labile DOC can be observed at the production sites; semi-labile species accumulate in the surface ocean, while deep-ocean DOC concentration and composition are relatively uniform. Recalcitrant DOM, i.e. forms of DOM not easily accessed and broken down by microbes, is thought to be distributed evenly throughout the water column (Hansell, 2013).

In oceanic subtropical gyres, covering more than 60% of the global ocean surface waters (Karl, 2002), dissolved organic matter (DOM) accumulates in the photic layer of the central gyre waters to concentrations often exceeding 70 μmol L−1 (Hansell et al., 2009; Raimbault et al., 2008). The South Pacific Gyre (SPG), the largest of the world's oceanic gyre systems, exhibits the most extreme oligotrophic conditions (Dandonneau et al., 2006): Nitrate-deplete waters with concentrations always below 0.01 μmol L−1 (Raimbault et al., 2008) lead to year-round low chlorophyll a concentrations not exceeding 0.03 μg L−1 and the clearest waters of the world's ocean (Claustre and Maritorena, 2003; Morel et al., 2007). CO2 fixation rates from nitrate-based new production or dinitrogen fixation are low (Raimbault and Garcia, 2008; Shiozaki et al., 2018). An interplay of many factors is hypothesized to contribute to DOM accumulation. Nutrient limitation and associated DOC overproduction have been proposed (Biersmith and Benner, 1998; Thingstad et al., 1997). Along similar lines, Raimbault et al. (2008) suggest that low primary production, restricted by nutrient supply, can lead to the accumulation of C-rich organic matter in the closed ecosystem of the central gyre waters due to weak lateral advection and preferential removal of N- and P-moieties from dissolved organics (Letscher and Moore, 2015). Limited availability of nitrogen, but not iron, and labile carbon sources were previously experimentally identified as impairing heterotrophic growth in the southern Pacific (Van Wambeke et al., 2008). Other studies have attributed the accumulation of semi-labile DOM in surface gyre waters mainly to vertical stratification (Goldberg et al., 2010; Hansell et al., 2009; Skoog and Benner, 1997). On molecular level, strong solar irradiation of the clear, low latitude waters may produce intrinsically stable DOM compounds via photohumification (Benner and Biddanda, 1998; Obernosterer and Benner, 2003; Obernosterer et al., 1999), leading to an accumulation of recalcitrant DOC. In addition to the intrinsic stability of certain structures in DOM, the high dilution of single compounds below a metabolically profitable threshold or environmental constraints, e.g. through lack of nutrients, have been hypothesized to contribute to the millennial-scale stability in the oceans (Arrieta et al., 2015; Dittmar, 2014; Jiao et al., 2011; Mentges et al., 2019).

DOC in the oceans makes up one of the largest actively cycled carbon pools on earth (Williams and Druffel, 1987). The bulk C concentrations of the DOM pool can be quantified via high temperature catalytic combustion or wet chemical oxidation through detection of CO2 released from organically bound C (Menzel and Vaccaro, 1964; Ogawa and Ogura, 1992; Sharp et al., 2002). Thus, initial conclusions about reactivity and source of the organic matter can be drawn from distribution of DOC concentrations, if analyzed over spatial or temporal gradients. Few biomolecules are directly recognizable in DOM, of which amino acids and neutral sugars are readily utilized by heterotrophic microbes (Jørgensen et al., 2014). Solid-phase extraction (SPE), especially using PPL columns (Dittmar et al., 2008), has become the most commonly applied method to extract and concentrate DOM from water samples for subsequent untargeted mass spectrometric analyses (Green et al., 2014). PPL-SPE biases against very small and polar molecules and colloids (Perminova et al., 2014; Raeke et al., 2016; Sleighter and Hatcher, 2008), and is considered to more representatively extract the recalcitrant DOM pool (Hansman et al. 2015), although it does capture recently produced DOM as well (Wienhausen et al., 2017). Fourier-transform ion cyclotron resonance mass spectrometry (FT-ICR-MS, Comisarow and Marshall, 1974; Marshall et al., 1998) of SPE-DOM has become a widely applied approach in marine biogeochemical studies. Across oceans, FT-ICR-MS has successfully been employed to investigate DOM molecular mass; heteroelement content; degree of oxidation or aromaticity; as well as turnover estimates of DOM subpools due to microbial or photochemical processing (Hansman et al. 2015; Landa et al., 2018; Medeiros et al., 2016; Stubbins and Dittmar, 2015). Yet, little is known about the molecular composition of DOM accumulating in subtropical gyres. The high precision and mass accuracy of the FT-ICR-MS allow the assignment of molecular formulas to tens of thousands of compounds in highly complex mixtures (Marshall et al., 2013; Kind and Fiehn, 2007; Koch et al., 2005; Smith et al., 2018). Improving the computationally intensive molecular formula attribution process is a field of ongoing research; a general challenge is that the accuracy of mass determination decreases with mass, while the number of possible formula assignments increases. Different approaches, based on in-house developed routines or using a variety of free or commercially available programs, can be taken to maximize the reliability of the molecular formula assignments. In this study, we integrate a comparison between two molecular formula assignment pipelines following FT-ICR-MS data collection (Supplemental Fig. S1): For the first approach, the magnitude mode spectrum is analyzed. In magnitude mode, the most widely applied mode of operation in natural organic matter studies (Da Silva et al., 2020), the time-domain data is converted to the frequency domain using the magnitude from the Fourier transformation. Molecular formulas are then assigned to the accurate masses within a certain error range, making use of spectra alignment, recalibration, and considering specific conditions regarding elemental and isotope ratios (Merder et al., 2020). In the second approach, the absorption mode processing, the phase of the ions is known and taken into account for the conversion to the frequency domain (Kilgour et al., 2013). This increases the resolving power, mass accuracy and sensitivity (Marshall et al., 1979), but phase correction must be performed carefully (Kilgour and Van Orden, 2015; Qi et al., 2011). The absorption mode processing is then followed by formulaic assignment by inference, through a network of homologous series, constructed from the mass differences between detected peaks in the mass spectra.

During the SO245 UltraPac expedition (Process oriented biogeochemical, microbiological, and ecological investigations of the ultraoligotrophic South Pacific Gyre), on board the RV Sonne, we passed through the most oligotrophic, central SPG waters (Fig. 1). The >8000 km transect from Chile to New Zealand was the first sampling campaign covering the whole South Pacific from East to West since the BIOSOPE cruise in 2004 (Claustre et al., 2008). Along the zonal transect, we examined the basin-wide dissolved organic matter distribution and composition and appraise the value and limitations of captured carbon fractions in context of environmental interpretation to better understand the reasons behind DOM accumulation in the subtropical gyre waters from a molecular point of view. Focusing on the upper water column, we combined FT-ICR-MS-derived heteroelement contributions and structural indices with physical and chemical oceanography to maximize our understanding of DOM cycling in the oligotrophic South Pacific.

Section snippets

Materials and methods

Water samples were obtained along a transect from Antofagasta (Chile) to Wellington (New Zealand) on the R/V Sonne cruise SO245 in the austral summer of 2015/2016. Water samples were retrieved from different water depths at 15 stations, alternating between deep (to bottom water, even numbered stations and station 15) and intermediate stations (to 500 m water depth, odd numbered stations, Fig. 1), using 12 L Niskin bottles attached to a conductivity, temperature and depth (CTD) probe (Seabird

Molecular formula attribution to ultrahigh-resolution mass spectrometry data

We found an overall high agreement between FT-ICR-MS datasets processed using magnitude-mode (MAG) and absorption-mode (AMP) approaches. Our final datasets included a lower number of molecular formula assignments in MAG (n = 7860) compared to AMP (n = 8821) when considering the same mass range and elemental attribution, as well as the post-processing steps described above. Da Silva et al. (2020) also assigned more peaks in AMP compared to MAG in a riverine sample reference when selecting the

Basin-scale diagenetic processing of DOM

Across ocean basins, upwelling and nutrient inputs from land increase auto- and heterotrophic DOC production in coastal areas, whereas heterotrophic utilization during water mass transport, and ageing in deeper water layers influence longitudinal distributions. Surface DOC concentrations exceeding deep ocean values are prevalent in most oceanic basins, due to photosynthetic production in the warmer, sunlit surface waters (Hansell et al., 2009) similar to those previously reported for the South

Conclusion

Distribution of DOC concentrations across the South Pacific indicated slow microbial degradation and a considerable DOC accumulation in the central gyre surface waters. The highly similar molecular fingerprint reflected photochemical reworking and preferential utilization of DON. Unexpected were the high similarity to surface water DOM outside the gyre and a high potential lability of the accumulated material. Our first assessment of the molecular-level composition of central gyre DOM provides

Declaration of competing interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Acknowledgements

We are most grateful to Captain L. Mallon, the crew and scientific party of SO245 who made work on board a great experience. We thank I. Ulber and M. Friebe (DOC/TDN quantification), K. Klaproth (FT-ICR-MS), and R. Weinert (carbohydrates) for help in the laboratory. X. Anton Alvarez-Salgado provided helpful comments on earlier versions of the manuscript. The UltraPac Expedition SO245 was funded by the Federal Ministry of Education and Research of Germany (Grant 03G0245A).

References (115)

  • N. Hertkorn

    Characterization of a major refractory component of marine dissolved organic matter

    Geochim. Cosmochim. Acta

    (2006)
  • D.M. Karl

    Nutrient dynamics in the deep blue sea

    Trends Microbiol.

    (2002)
  • B.P. Koch et al.

    Molecular formulae of marine and terrigenous dissolved organic matter detected by electrospray ionization Fourier transform ion cyclotron resonance mass spectrometry

    Geochim. Cosmochim. Acta

    (2005)
  • O.J. Lechtenfeld

    Molecular transformation and degradation of refractory dissolved organic matter in the Atlantic and Southern Ocean

    Geochim. Cosmochim. Acta

    (2014)
  • H.-Y. Li

    The chemodiversity of paddy soil dissolved organic matter correlates with microbial community at continental scales

    Microbiome

    (2018)
  • S. Matallana-Surget

    Response to UVB radiation and oxidative stress of marine bacteria isolated from South Pacific Ocean and Mediterranean Sea

    J. Photochem. Photobiol. B Biol.

    (2012)
  • D.W. Menzel

    The role of in situ decomposition of organic matter on the concentration of non-conservative properties in the sea

    Deep-Sea Res. Oceanogr. Abstr.

    (1970)
  • K. Mopper et al.

    Chapter 8 - marine photochemistry of organic matter: processes and impacts

  • N. Ogura

    The relation between dissolved organic carbon and apparent oxygen utilization in the Western North Pacific

    Deep-Sea Res. Oceanogr. Abstr.

    (1970)
  • C. Santinelli et al.

    Carbon isotope measurements reveal unexpected cycling of dissolved organic matter in the deep Mediterranean Sea

    Mar. Chem.

    (2015)
  • J.H. Sharp

    Final dissolved organic carbon broad community intercalibration and preliminary use of DOC reference materials

    Mar. Chem.

    (2002)
  • N. Silva et al.

    Water masses in the Humboldt current system: properties, distribution, and the nitrate deficit as a chemical water mass tracer for equatorial subsurface water off Chile

    Deep-Sea Res. II Top. Stud. Oceanogr.

    (2009)
  • L.I. Aluwihare et al.

    Two chemically distinct pools of organic nitrogen accumulate in the ocean

    Science

    (2005)
  • A.R. Arellano et al.

    Differential effects of solid-phase extraction resins on the measurement of dissolved lignin-phenols and organic matter composition in natural waters

    Limnol. Oceanogr. Methods

    (2018)
  • J.M. Arrieta

    Dilution Limits Dissolved Organic Carbon Utilization in the Deep Ocean

    (2015)
  • J.E. Bauer et al.

    14C activity of dissolved organic carbon fractions in the north-central Pacific and Sargasso Sea

    Nature

    (1992)
  • R. Benner et al.

    Photochemical transformations of surface and deep marine dissolved organic matter: effects on bacterial growth

    Limnol. Oceanogr.

    (1998)
  • T. Berman et al.

    Dissolved organic nitrogen: a dynamic participant in aquatic ecosystems

    Aquat. Microb. Ecol.

    (2003)
  • S. Bonnet

    Nutrient limitation of primary productivity in the Southeast Pacific (BIOSOPE cruise)

    Biogeosciences

    (2008)
  • S. Bonnet et al.

    Hot spot of N<sub>2</sub> fixation in the western tropical South Pacific pleads for a spatial decoupling between N<sub>2</sub> fixation and denitrification

    Proc. Natl. Acad. Sci.

    (2017)
  • M.L. Calleja et al.

    Dissolved organic carbon contribution to oxygen respiration in the central Red Sea

    Sci. Rep.

    (2019)
  • B.J. Campbell et al.

    Activity of abundant and rare bacteria in a coastal ocean

    Proc. Natl. Acad. Sci. U. S. A.

    (2011)
  • H. Claustre et al.

    The many shades of ocean blue

    Science

    (2003)
  • H. Claustre et al.

    Introduction to the special section bio-optical and biogeochemical conditions in the South East Pacific in late 2004: the BIOSOPE program

    Biogeosciences

    (2008)
  • M.P. Da Silva et al.

    Absorption mode spectral processing improves data quality of natural organic matter analysis by Fourier-transform ion cyclotron resonance mass spectrometry

    J. Am. Soc. Mass Spectrom.

    (2020)
  • J. D’Andrilli et al.

    An ultrahigh-resolution mass spectrometry index to estimate natural organic matter lability

    Rapid Commun. Mass Spectrom.

    (2015)
  • T. Dittmar

    Reasons behind long-term stability of dissolved organic matter

  • T. Dittmar et al.

    A simple and efficient method for the solid-phase extraction of dissolved organic matter (SPE-DOM) from seawater

    Limnol. Oceanogr. Methods

    (2008)
  • E.R.M. Druffel et al.

    Radiocarbon in dissolved organic carbon of the South Pacific Ocean

    Geophys. Res. Lett.

    (2015)
  • C. Fasching et al.

    Hydrology controls dissolved organic matter export and composition in an Alpine stream and its hyporheic zone

    Limnol. Oceanogr.

    (2016)
  • T.G. Ferdelman et al.

    Nutrient Data from CTD Nisken Bottles from Sonne Expedition SO-245 “UltraPac”

    (2019)
  • T.G. Ferdelman

    Calibrated Dissolved O2 Data from RV Sonne Expedition SO245 “UltraPac”

    (2019)
  • R. Flerus

    A molecular perspective on the ageing of marine dissolved organic matter

    Biogeosciences

    (2012)
  • P. Flombaum

    Present and future global distributions of the marine Cyanobacteria Prochlorococcus and Synechococcus

    Proc. Natl. Acad. Sci.

    (2013)
  • L. Gomez-Consarnau et al.

    Structuring of bacterioplankton communities by specific dissolved organic carbon compounds

    Environ. Microbiol.

    (2012)
  • D. Graeber

    Technical note: comparison between a direct and the standard, indirect method for dissolved organic nitrogen determination in freshwater environments with high dissolved inorganic nitrogen concentrations

    Biogeosciences

    (2012)
  • H. Halm

    Heterotrophic organisms dominate nitrogen fixation in the South Pacific Gyre

    ISME J.

    (2012)
  • D.A. Hansell

    Recalcitrant dissolved organic carbon fractions

    Annu. Rev. Mar. Sci.

    (2013)
  • D.A. Hansell et al.

    Deep-ocean gradients in the concentration of dissolved organic carbon

    Nature

    (1998)
  • D.A. Hansell et al.

    Dissolved organic matter in the ocean - a controversy stimulates new insights

    Oceanography

    (2009)
  • Cited by (17)

    • Influence of the conservation mode of seawater for dissolved organic carbon analysis

      2022, Marine Environmental Research
      Citation Excerpt :

      For DOM study, samples are often extracted onboard using the solid phase extraction procedure of Dittmar et al. (2008). Methanol extracts are then again flame sealed in glass ampoules and frozen until analysis (Osterholtz et al., 2021). For the trace metal community, the filtration of samples onto polyethylsulfone filters and their acidification after their collection in acid clean HDPE bottles is commonly used for sample preservation during offshore campaign.

    • Oxygen availability driven trends in DOM molecular composition and reactivity in a seasonally stratified fjord

      2022, Water Research
      Citation Excerpt :

      However, DOM is a highly heterogeneous mixture of presumably millions of different compounds (Dittmar, 2015), changes of which at molecular level can bring about differences in reactivity and persistence of DOM in the ocean that are not detectable on the bulk concentration or composition level (Bercovici et al., 2018; Shen and Benner, 2020; Walker et al., 2016). Fourier transform ion cyclotron resonance mass spectrometry (FT-ICR MS) has emerged as a valuable tool through which one can obtain detailed information on individual compound in the ultra-complex organic matter, and successfully provided insights into the molecular composition of DOM in diverse environments (e.g., Cai et al. 2019, He et al. 2019, Kellerman et al. 2014, Lehmann et al. 2020, Letourneau et al. 2021, Osterholz et al. 2021). To move further forward, we need to better understand the impact of deoxygenation on the molecular properties of DOM, especially in the chemical composition and structure.

    View all citing articles on Scopus
    View full text