Perspectives on the microbial carbon pump with special reference to microbial respiration and ecosystem efficiency in large estuarine systems

Abstract

Abstract. Although respiration-based oxidation of reduced carbon releases CO 2 into the environment, it provides an ecosystem with the metabolic energy for essential biogeochemical processes, including the newly proposed microbial carbon pump (MCP). The efficiency of MCP in heterotrophic microorganisms is related to the mechanisms of energy transduction employed and hence is related to the form of respiration utilized. Anaerobic organisms typically have lower efficiencies of energy transduction and hence lower efficiencies of energy-dependent carbon transformation. This leads to a lower MCP efficiency on a per-cell basis. Substantial input of terrigenous nutrients and organic matter into estuarine ecosystems typically results in elevated heterotrophic respiration that rapidly consumes dissolved oxygen, potentially producing hypoxic and anoxic zones in the water column. The lowered availability of dissolved oxygen and the excessive supply of nutrients such as nitrate from river discharge lead to enhanced anaerobic respiration processes such as denitrification and dissimilatory nitrate reduction to ammonium. Thus, some nutrients may be consumed through anaerobic heterotrophs, instead of being utilized by phytoplankton for autotrophic carbon fixation. In this manner, eutrophied estuarine ecosystems become largely fueled by anaerobic respiratory pathways and their efficiency is less due to lowered ecosystem productivity when compared to healthy and balanced estuarine ecosystems. This situation may have a negative impact on the ecological function and efficiency of the MCP which depends on the supply of both organic carbon and metabolic energy. This review presents our current understanding of the MCP mechanisms from the view point of ecosystem energy transduction efficiency, which has not been discussed in previous literature.

Microbial Surface Colonization and Biofilm Development in Marine Environments

“…On the other hand, POC degradation by surface-colonizing microorganisms may also release recalcitrant DOC (209), facilitating carbon sequestration by the microbial carbon pump mechanism ( Fig. 1) (272,(282)(283)(284)(285). DOC (up to 662 Pg C) forms the largest organic carbon pool in the modern ocean, and a substantial fraction (ϳ97%) of DOC consists of refractory and ultrarefractory molecules that persist for thousands of years in the marine environment (286).…”

“…DOC (up to 662 Pg C) forms the largest organic carbon pool in the modern ocean, and a substantial fraction (ϳ97%) of DOC consists of refractory and ultrarefractory molecules that persist for thousands of years in the marine environment (286). The quantitative contributions of surface-associated microorganisms to the size and dynamics of the ocean's POC and DOC reservoirs and the influence of spatiotemporally different environmental conditions on surface-associated microbial processes and activities are still poorly understood, especially under anthropogenic perturbation and global change scenarios (16,(284)(285)(286). In-depth studies of the marine surface-associated microbiota are fundamental for a mechanistic and predictive understanding of the marine carbon cycle.…”

“…Oxygen-limited and oxygen-depleted conditions facilitate various microaerophilic and anaerobic chemolithoautotrophic carbon fixation and heterotrophic respiration and fermentation processes (147,302,303). Different respiration pathways have distinctly different energy conservation efficiencies (147,304), and hypoxic and anoxic conditions usually exert a negative influence on respiratory efficiency and thus the carbon sequestration efficiency of the ocean (284,285). Furthermore, the increasing impacts of anthropogenic activities and global warming have also caused estuarine and coastal waters (including polar ocean coastal areas) to become more eutrophic and conversely have caused open oceans, particularly the giant subtropical gyres of the Pacific and Atlantic Oceans, to become more oligotrophic (305)(306)(307)(308)(309)(310).…”

“…Two-component signal transduction systems (TCSs) are very common in both Bacteria and Archaea (284,345,346). These systems enable microorganisms to constantly sense and respond to environmental changes and stresses, such as those caused by the availability of inorganic nutrients and metabolizable organic substrates, temperature, pH, O 2 , redox potential, light intensity, osmolarity, and toxins, including reactive oxygen and nitrogen species as well as other substances (347).…”

Mechanisms of microbial carbon sequestration in the ocean – future research directions

“…6). Anthropogenic eutrophication in estuarine and coastal areas may thus reduce the efficiency of the MCP (Dang and Jiao, 2014). This reduced efficiency may be exacerbated by the potential "priming" effect of labile organic matter addition stimulating the respiration of RDOC, as recently seen in soil environments (Wieder et al, 2013).…”