Microbial control of the dark end of the biological pump

Abstract

A fraction of the carbon captured by phytoplankton in the sunlit surface ocean sinks to depth as dead organic matter and faecal material. The microbial breakdown of this material in the subsurface ocean generates carbon dioxide. Collectively, this microbially mediated flux of carbon from the atmosphere to the ocean interior is termed the biological pump. In recent decades it has become clear that the composition of the phytoplankton community in the surface ocean largely determines the quantity and quality of organic matter that sinks to depth. This settling organic matter, however, is not sufficient to meet the energy demands of microbes in the dark ocean. Two additional sources of organic matter have been identified: non-sinking organic particles of debated origin that escape capture by sediment traps and exhibit stable concentrations throughout the dark ocean, and microbes that convert inorganic carbon into organic matter. Whether these two sources can together account for the significant mismatch between organic matter consumption and supply in the dark ocean remains to be seen. It is clear, however, that the microbial community of the deep ocean works in a fundamentally different way from surface water communities.

Figure 1. The biological pump

Phytoplankton in the euphotic zone fix carbon dioxide using solar energy. The particulate organic carbon (POC) produced is grazed on by herbivorous zooplankton, or consumed directly or indirectly by heterotrophic microbes feeding on solubilized remains of phytoplankton. Between 1 and 40% of the primary production is exported out of the euphotic zone, and it exponentially attenuates towards the base of the mesopelagic zone at around 1,000 m depth. Remineralization of organic matter in the oceanic water column converts the organic carbon back to carbon dioxide. Only about 1% of the surface production reaches the sea floor.

Figure 2. Sinking velocity of different phytoplankton size classes

Average sinking velocity versus time (in days) for phytoplankton cells with initial diameters of 1, 3, 10, 30 and 100 μm. Algal cells are considered to collide, forming aggregates at rates that depend on their abundance and size. Large cells settle faster than small ones. With time, cell concentrations increase, causing an increase in the fraction of material in aggregates. The resulting increase in average particle size leads to an increase in average settling speed with time. Peaks in total cell concentration occur when enhanced losses due to settling balance gains due to cell division. The maximum average settling rate of particles formed from 1 μm cells is not substantially different from that of particles formed from 30 μm cells. Reproduced with permission from ref. , © 2007 AAAS.

Figure 3. Processes affecting the flux of particles in the ocean

The widths of the coloured surfaces in the euphotic zone represent the relative contribution of different phytoplankton size classes to particle export under nutrient-poor and nutrient-rich conditions. The aggregate size and the slope b increase from oligotrophic to eutrophic systems. This transition is due to an overall community shift from picoplankton (size range 0.2-2 μm) to nanoplankton (2-20 μm) and microplankton (20-200 μm). Below the euphotic zone, microbial or zooplankton degradation alters the initial particulate organic carbon flux indicated by the curve (red lines) using the typical slope values (b) found for oligotrophic (b = 0.2) or eutrophic (b = 1) ocean regions. Modified with permission from ref. , © 2009 Association for the Sciences of Limnology and Oceanography.

Figure 4. Model relating the export efficiency to the transfer efficiency of the biological pump

Low export efficiencies indicate that most of the attenuation of net primary production is already taking place in the euphotic zone. Low transfer efficiencies suggest rapid reduction of particulate organic material between the base of the euphotic zone and 100 m below. The circle sizes are proportional to the magnitude of net primary production. The contour lines from 1 to 40% represent the flux of export production as a function of euphotic zone export and transfer efficiency. Arrows of parameters along the y and x axes indicate some processes that would move a particular oceanic site higher or lower on these scales. NA, North Atlantic; SP, South Pacific; NWP, northwest Pacific; NEP, northeast Pacific; SUP, subtropical Pacific; TP, tropical Pacific. The numbers attached to the region names indicate different sites or seasons. Modified with permission from ref. , © 2009 Association for the Sciences of Limnology and Oceanography.

Figure 5. Microbial carbon demand and particulate carbon flux in the mesotrophic and oligotrophic North Atlantic

a, Depth-dependent microbial biomass production, as measured by carbon uptake. b, Microbial carbon demand based on measured biomass production and applying an average open-ocean microbial growth efficiency of 20%. c, Microbial carbon demand based on measured biomass production and a measured microbial growth efficiency for the dark ocean of 2% according to ref. . Also shown is the depth-dependent particle flux calculated from a model (from ref. 52) using primary production values reflecting the mesotrophic and oligotrophic North Atlantic. In b and c, dissolved inorganic carbon fixation by microbes is added to the output of the flux model assuming that chemolithoautrophy represents a fresh source of non-sinking organic carbon in the dark ocean. Data from T. Reinthaler et al., unpublished.

Figure 6. Microbial inorganic carbon fixation and microbial heterotrophic production in the North Atlantic

a,b, Dissolved inorganic carbon (DIC) fixation and heterotrophic production in the eastern (a) and western (b) North Atlantic basin. Black dots indicate the latitudes and depths where samples were collected. Black contour lines and related numbers indicate rates (μmol C m⁻³ d⁻¹). Reproduced with permission from ref. , © 2010 Elsevier.