Speed bumps and barricades in the carbon cycle: substrate structural effects on carbon cycling

The observation that a fraction of organic matter produced in marine systems evades the concerted efforts of microbial communities and is buried in sediments suggests that there are ‘speed bumps’ in carbon degradation pathways that impede microbially driven remineralization processes. The initial step in degradation of macromolecules, extracellular enzymatic hydrolysis, is often stated to be ‘the’ rate-limiting step in carbon remineralization. Experimental investigations described here, however, demonstrate that at least in certain cases, microbes produce extracellular enzymes on time scales of hours to tens of hours in response to substrate addition, and hydrolysis is extremely rapid. If enzymatic hydrolysis can be rapid, what factors slow or stop organic matter degradation? A lack of the correct inducer to initiate enzyme production, and/or a lack of the correct organism to produce the required enzyme, may result in a complete lack of hydrolysis in certain environments—a barricade, rather than a speed bump. Preliminary evidence supporting this hypothesis includes a comparison of polysaccharide hydrolysis in seawater and sediments, which demonstrates that the spectrum of enzymes active in seawater and sediments are fundamentally different. Furthermore, a survey of enzyme activities in surface waters from a range of locations suggests that pelagic microbial communities also differ widely in their abilities to express specific extracellular enzymes. Trans-membrane transport through porins is yet another potential location of structure-related selectivity. Our efforts to identify speed bumps and barricades are hampered by our inability to structurally characterize in sufficient detail the macromolecular structures present in marine systems. Furthermore, assessments of organic matter ‘quality’ from a chemical perspective do not necessarily accurately reflect the availability of organic carbon to microbial communities. For these communities, in fact, ‘quality’ may be a variable, which depends on the enzymatic and uptake capabilities of community members. To begin to assess substrate structure and quality from a microbial perspective, we will have to combine specific knowledge of macromolecular structures with detailed investigations of the enzymatic and transport capabilities of heterotrophic marine microbes.