Elsevier

Progress in Oceanography

Volume 134, May 2015, Pages 432-450
Progress in Oceanography

Review
The microbial carbon pump concept: Potential biogeochemical significance in the globally changing ocean

https://doi.org/10.1016/j.pocean.2015.01.008Get rights and content

Highlights

  • The biological carbon pump sequesters carbon (C) by vertical transfer to deep ocean.

  • The microbial carbon pump (MCP) sequesters C by producing DOC with lifetime >100 years.

  • We define the magnitude of the MCP as the rate of production of DOC>100.

  • Our novel estimate of the magnitude of the MCP in the World Ocean is 0.2 Pg C year−1.

  • Of 7 predicted climate-related ocean changes, 3 could enhance C sequestration by MCP.

Abstract

Three vertical ocean carbon pumps have been known for almost three decades to sequester atmospheric carbon in the deep-water and sediment reservoirs, i.e. the solubility pump, the carbonate pump, and the soft-tissue (also known as organic, or biological) carbon pump (BCP). These three pumps maintain the vertical gradient in total dissolved inorganic carbon between the surface and deep waters. The more recently proposed microbial carbon pump (MCP) would maintain a gradient between short- and long-lived dissolved organic carbon (DOC; average lifetimes of <100 and >100 years, respectively). Long-lived DOC is an additional proposed reservoir of sequestered carbon in the ocean. This review: examines critically aspects of the vertical ocean carbon pumps and the MCP, in particular their physical dimensions and their potential roles in carbon sequestration; normalises the dimensions of the MCP to allow direct comparisons with the three vertical ocean carbon pumps; compares the MCP and vertical ocean carbon pumps; organises in a coherent framework the information available in the literature on refractory DOC; explores the potential effects of the globally changing ocean on the MCP; and identifies the assumptions that generally underlie the MCP studies, as bases for future research. The study: proposes definitions of terms, expressions and concepts related to the four ocean carbon pumps (i.e. three vertical pumps and MCP); defines the magnitude for the MCP as the rate of production of DOC with an average lifetime of >100 years and provides its first estimate for the World Ocean, i.e. 0.2 Pg C year−1; and introduces an operational “first-time-sequestration” criterion that prevents organic carbon fluxes from being assigned to both the BCP and the MCP. In our review of the potential effects of predicted climate-related changes in the ocean environment on the MCP, we found that three of the seven predicted changes could potentially enhance carbon sequestration by the MCP, and three could diminish it.

Introduction

In the World Ocean, there is a strong vertical gradient in the concentration of dissolved CO2, and there are several different forms that make up total dissolved inorganic carbon (CT):CT=CO2(dissolved)+H2CO3+HCO3-+CO32-where H2CO3, HCO3 and CO32− are carbonic acid, and bicarbonate and carbonate ions, respectively. In the literature, CT is also called dissolved inorganic carbon (DIC) and total CO2 (TCO2 or ∑CO2). The global mean CT in deep waters below 1200 m is higher than in the surface mixed layer, i.e. 2284 and 2012 μmol kg−1, respectively (Volk and Hoffert, 1985, and Fig. 1). This requires that physical, chemical and biological processes counteract the continuous erosion by diffusive ocean mixing (on timescale of ∼1000 years) of the vertical differences in the concentration of CT. Volk and Hoffert (1985) referred to the processes that maintain the CT gradient in the World Ocean as the “ocean carbon pumps”, and these pumps have an important effect on the air–sea CO2 fluxes on century timescales (IPCC, 2013, Section 6.3.2.5.5).

In their seminal paper, Volk and Hoffert (1985) defined three vertical ocean carbon pumps, corresponding to different forms of carbon in the marine environment: the solubility pump for CT, the carbonate pump for particulate inorganic carbon (CaCO3), and the soft-tissue pump (also called organic carbon pump, but more generally biological carbon pump) for particulate organic carbon (POC) although this pump can also include dissolved organic carbon (DOC). The expression “biological carbon pump” (BCP) refers to either the organic component of the ocean carbon pump only, or both the organic and CaCO3 components. Volk and Hoffert (1985) and Passow and Carlson (2012) used biological carbon pump for the sum of the two components. In this review, BCP refers only to the organic component, consistent with the Glossary in IPCC (2013, Annex III).

Recently, another ocean carbon pump, called the microbial carbon pump (MCP), was proposed by Jiao and collaborators (Jiao et al., 2010, Jiao et al., 2011, Jiao and Azam, 2011). The MCP concept was developed within the context of marine microbiology with proposed links with marine biogeochemistry. A key assumption of the MCP is that the production mechanisms of long-lived DOC in the ocean are largely microbial. In contrast, the BCP concept was mostly developed, studied and modelled within the context of marine food webs and ocean biogeochemistry. The BCP has been central to studies that explore the present and future responses of biogeochemical fluxes to the globally changing ocean, which are critical to help inform governmental policy decisions (e.g. Passow and Carlson, 2012). If the oceanographic community is to consider the MCP along with the other ocean carbon pumps in assessments of the biologically mediated biogeochemical fluxes of carbon in the changing ocean, it is important that the MCP concept be expressed in the same units as the three other ocean carbon pumps (i.e. normalised).

Although well accepted now, the three vertical ocean carbon pumps were, at their origin, conceptual constructions that were based on a few observations and aimed at providing frameworks for the development and testing of hypotheses and models. This was clear in the seminal paper of Volk and Hoffert (1985), e.g. “distinguishing the strengths and efficiencies of the pumps may help formulate questions about models and possible ocean changes in the future”. Similarly in the recent paper of Jiao et al. (2010), the authors proposed “the microbial carbon pump as a conceptual framework to address the role of microbial generation of RDOM and relevant carbon storage”. The vertical ocean carbon pumps concept was proposed almost 30 years ago whereas the MCP concept is quite recent, hence the first now rests on extensive quantitative evidence (e.g. Sarmiento and Gruber, 2006) and has produced well accepted numerical models (e.g. Kwon et al., 2009), whereas the second (e.g. DeVries et al., 2014) is still largely hypothetical.

In the literature, expressions such as ocean carbon pump (biological, carbonate, organic, soft tissue, or solubility), carbon export and carbon sequestration are often used by authors differently, hence potentially creating confusion. Here, we propose and define a coherent set of expressions for use by the research community. The acronyms and symbols of quantities, their definitions and areal dimensions, and the corresponding units are summarised in Table 1. For easy reference, the definitions proposed in the text are assembled in a logical framework in Table 2, and schematised in Fig. 2. Our definitions are largely consistent with those of Passow and Carlson (2012). For the different fractions of dissolved organic carbon, we use the definitions proposed by Hansell (2013). Because our study examines ocean carbon pumps, we will refer below to DOC and POC instead of dissolved and particulate organic matter (DOM and POM, respectively).

A recent paper by Jiao et al. (2014) presented a general overview of the field and addressed future research directions for studies on the MCP based primarily on microbiological considerations. The objectives of the present in depth review are sequentially to: (1) critically examine key aspects of the vertical ocean carbon pumps, in particular their physical dimensions and their roles in carbon sequestration; (2) critically examine key aspects of the MCP, and normalise its dimensions to allow direct comparisons with the three vertical ocean carbon pumps; (3) compare the MCP with the vertical ocean carbon pumps; (4) organise in a coherent framework the information available on refractory dissolved organic carbon; (5) explore the potential effects of the globally changing ocean on the MCP; and (6) identify the assumptions that generally underlie the MCP studies, as bases for future research.

In the following sections, we briefly describe and compare the functioning of the three vertical ocean carbon pumps, and examine carbon sequestration in the ocean, the DOC fractions and the microbial carbon pump. We then compare the microbial and the vertical ocean carbon pumps, review reports of refractory dissolved organic carbon processes in the ocean, and examine potential effects of climate change on the microbial carbon pump. We conclude by reviewing the main assumptions found in the major publications on the MCP.

Section snippets

The three vertical ocean carbon pumps

The carbon processed by the three vertical ocean carbon pumps originates in the atmosphere. The dissolution of atmospheric CO2 into the upper ocean is represented by downward-pointing arrow ➊ in Fig. 2 (the numbers in full or open circles in this section refer to arrows in Fig. 2). The steps of the solubility pump are as follows. Firstly, dissolved atmospheric CO2 in surface waters combines with water molecules (H2O), which produces bicarbonate and carbonate ions (HCO3 and CO32−, respectively)

Ocean carbon sequestration

The vertical ocean carbon pumps have an important effect on the air–sea CO2 fluxes on century timescales (IPCC, 2013, Section 6.3.2.5.5). The carbon pumps contribute to carbon sequestration, which is defined as the addition of inorganic or organic carbon to a terrestrial or aquatic reservoir (i.e. to a component of the climate system other than the atmosphere), where a reservoir has the capacity to accumulate, store or release carbon (here, the definition of “carbon sequestration” and

DOC fractions: lifetimes and production rates

In the ocean, there is co-occurrence of different DOC fractions with different lifetimes. As reported in Jiao et al. (2014), the lifetime of a substance is defined as the time for its concentration to decrease to 1/e of its initial value, i.e. 1/e = 0.37, which assumes exponential decay. This corresponds to the concept of “e-folding lifetime”, which differs from the related concept of “half-life” where 1/2 is used instead of 1/e.

Here, we refer to the five DOC fractions defined by Hansell (2013,

The microbial and solubility carbon pumps

The solubility pump sequesters carbon by transferring CT downwards, the first step being the dissolution of atmospheric CO2 in the upper ocean, followed by deep mixing of the CO2-rich water (Section ‘Ocean carbon sequestration’). As the concentration of atmospheric CO2 increases, more CO2 dissolves in surface-ocean waters, leading to increasing concentration of H+ in seawater (Eq. (2)), thus decreasing the pH. This is called ocean acidification. This change in the ocean carbonate chemistry may

Review of reports of refractory dissolved organic carbon processes in the ocean

The MCP proposal has prompted the publication of a number of syntheses and complementary papers on RDOC and the MCP (e.g. the 10 papers in Chapter 2 of Jiao et al., 2011, Jiao et al., 2014). Here, we briefly review and assess the MCP-relevant DOC information. The terms “refractory” or “recalcitrant” DOC or DOM (RDOC or RDOM) reported in some publications do not always correspond to the definition of RDOC given in Section ‘The three vertical ocean carbon pumps’ and used here, and may also often

Potential effects of climate change on the microbial carbon pump

The potential effects of climate change on the BCP were reviewed by Passow and Carlson (2012) and Turner (2015), and will therefore not be addressed here. The authors considered that the sequestration flux depends upon the input rates of allochthonous nutrients to the ocean (i.e. aeolian or fluvial inputs, or N2 fixation), the export flux at the base of the euphotic zone, the deviation from Redfield stoichiometry of both carbon fixation and remineralisation, and the flux attenuation in the upper

Conclusions

The above predictions about the responses of the MCP to changes in the marine environment caused by climate change were based on combining a limited number of empirical studies, for which data were often scarce, and assumptions, which were not always clearly stated. Assumptions are especially critical when data are not available or are contradictory. The mechanisms and processes examined in Sections ‘Production of refractory dissolved organic carbon in the ocean’, ‘Removal of refractory

Acknowledgements

We thank Craig A. Carlson, Tim DeVries, Jean-Pierre Gattuso, Richard S. Lampitt, Toshi Nagata, Uta Passow, Fereidoun Rassoulzadegan and Christian Tamburini for useful information related to our study, and Farooq Azam, Nianzhi Jiao, Susanne Neuer, Carol Robinson, Victor Smetacek and Helmuth Thomas for comments following the presentation of a short version of this work to Workshop 2 of the IMBIZO III meeting. We also thank the reviewers of the successive versions of our review for their numerous,

References (89)

  • R.M. Amon et al.

    Bacterial utilization of different size classes of dissolved organic matter

    Limnology and Oceanography

    (1996)
  • D. Archer et al.

    Ocean methane hydrates as a slow tipping point in the global carbon cycle

    Proceedings of the National Academy of Sciences of the United States of America

    (2009)
  • Azam, F., Jiao, N., http://science.imirus.com/Mpowered/book/vscim11/i2/p1, 2011. Revisiting the ocean’s carbon cycle....
  • R.T. Barber et al.

    A rising tide lifts all phytoplankton: growth response of other phytoplankton taxa in diatom-dominated blooms

    Global Biogeochemical Cycles

    (2006)
  • R. Benner et al.

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

    Limnology and Oceanography

    (1998)
  • Benner, R., Herndl, G.J., http://science.imirus.com/Mpowered/book/vscim11/i2/p1, 2011. Bacterially derived dissolved...
  • L. Bopp et al.

    Response of diatoms distribution to global warming and potential implications: a global model study

    Geophysical Research Letters

    (2005)
  • A. Capotondi et al.

    Enhanced upper-ocean stratification with climate change in the CMIP3 models

    Journal of Geophysical Research

    (2012)
  • C.A. Carlson

    Production and removal processes

  • Carlson, C.A., Hansell, D.A., Tamburini, C., http://science.imirus.com/Mpowered/book/vscim11/i2/p1, 2011. DOC...
  • P. Cermeño et al.

    The role of nutricline depth in regulating the ocean carbon cycle

    Proceedings of the National Academy of Sciences of the United States of America

    (2008)
  • DeVries, T.J., Primeau, F.W., Deursch, C.A., http://www.sgmeet.com/osm2014/viewabstract.asp?AbstractID=17345, 2014....
  • T. Dittmar et al.

    A heat-induced molecular signature in marine dissolved organic matter

    Nature Geoscience

    (2009)
  • S.C. Doney

    Plankton in a warmer world

    Nature

    (2006)
  • S.C. Doney et al.

    Ocean acidification: a critical emerging problem for the ocean sciences

    Oceanography

    (2009)
  • E.R.M. Druffel et al.

    Cycling of dissolved and particulate organic matter in the open ocean

    Journal of Geophysical Research

    (1992)
  • M. Eichinger et al.

    Consumption and release of dissolved organic carbon by marine bacteria in a pulsed-substrate environment: from experiments to modelling

    Aquatic Microbial Ecology

    (2009)
  • Eichinger, M., Poggiale, J.C., Sempéré, R., http://science.imirus.com/Mpowered/book/vscim11/i2/p1, 2011. Toward a...
  • P.G. Falkowski et al.

    Mix and match: how climate selects phytoplankton

    Nature

    (2007)
  • M.J.R. Fasham et al.

    Modeling the relative contributions of autotrophs and heterotrophs to carbon flow at a Lagrangian JGOFS station in the Northeast Atlantic: the importance of DOC

    Limnology and Oceanography

    (1999)
  • Z.V. Finkel et al.

    Phytoplankton in a changing world: cell size and elemental stoichiometry

    Journal of Plankton Research

    (2010)
  • M. Frankignoulle et al.

    Marine calcification as a source of carbon dioxide: positive feedback of increasing atmospheric CO2

    Limnology and Oceanography

    (1994)
  • J.P. Gattuso et al.

    Measurement of community metabolism and significance in the coral reef CO2 source-sink debate

    Proceedings of the National Academy of Sciences of the United States of America

    (1999)
  • D.F. Gruber et al.

    Dynamics and characterization of refractory dissolved organic matter produced by a pure bacterial culture in an experimental predator-prey system

    Applied and Environment Microbiology

    (2006)
  • Guidi, L., Uitz, J., Legendre, L., ms. An optical-based approach to estimate natural carbon sequestration in the deep...
  • D.A. Hansell

    Recalcitrant dissolved organic carbon fractions

    Annual Review of Marine Science

    (2013)
  • D.A. Hansell et al.

    Dissolved organic matter in the ocean: new insights stimulated by a controversy

    Oceanography

    (2009)
  • D.A. Hansell et al.

    Net removal of major marine dissolved organic carbon fractions in the subsurface ocean

    Global Biogeochemical Cycles

    (2012)
  • C. Heinze et al.

    Glacial pCO2 reduction by the world ocean: experiment with the Hamburg Carbon Cycle Model

    Paleoceanography

    (1991)
  • S.A. Henson et al.

    Global patterns in efficiency of particulate organic carbon export and transfer to the deep ocean

    Global Biogeochemical Cycles

    (2012)
  • H. Herzog et al.

    An issue of permanence: assessing the effectiveness of temporary carbon storage

    Climatic Change

    (2003)
  • S. Honjo et al.

    Understanding the role of the biological pump in the global carbon cycle: an imperative for ocean science

    Oceanography

    (2014)
  • IPCC, 2007. Climate Change 2007: Synthesis Report. Contribution of Working Groups I, II and III to the Fourth...
  • IPCC, 2013. Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment...
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