Encyclopedia of Geochemistry

Living Edition
| Editors: William M. White

Organic Matter Degradation and Preservation

  • Sandra ArndtEmail author
  • Douglas Edward LaRowe
Living reference work entry
DOI: https://doi.org/10.1007/978-3-319-39193-9_184-1

Definition

Organic matter degradation is the disintegration of mainly photosynthetically produced organic matter by microorganisms. It proceeds via multiple enzymatic reactions involving different microorganisms and oxidants as well as a number of intermediate compounds. Depending on the degradation pathway, organic matter is directly oxidized to carbon dioxide, partly oxidized to intermediate compounds or reduced to methane. In the simplest of terms, preservation can be simply defined as the incompleteness of degradation.

Global Importance

Life depends on the continuous recycling of bioactive elements. The resulting global biogeochemical cycles are intimately connected through the biological process of photosynthesis, which fixes energy in carbon bonds and respiration, which breaks the organic bonds and thereby releases energy. On long time scales, organic matter, OM, production generally exceeds respiration and a small fraction of the photosynthetically produced organic carbon escapes degradation to be preserved and buried in sediments (Berner 2003). This small imbalance between photosynthesis and respiration connects the short- and long-term carbon cycles , controls the long-term evolution of atmospheric CO2, and has enabled the accumulation of oxygen in the atmosphere (Berner 2003). However, compilations of field data reveal that OM production, degradation, and preservation rates vary significantly in space (Burdige 2007; Arndt et al. 2013) and time (Berner 2003). Understanding the processes that control the degradation and preservation of OM during transport and burial is important for predicting the impact and feedbacks of past, present, and future global change on global biogeochemical cycles and climate.

OM Degradation and Preservation in the Earth System

Organic matter represents the largest reactive reservoir of reduced carbon in the Earth system, divided between an estimated 1760 Pg C of soil OM, 1000 Pg C in recent surface sediments (excluding deep sediments), and 688 Pg C dissolved in the ocean (Eglinton and Repeta 2004). Almost all of the organic matter that is degraded or preserved in the Earth System originates from photosynthetic activity in the terrestrial (global net primary productivity, NPP = ~59 Pg C year−1) or marine biosphere (global NPP = ~49 Pg C year−1). In addition, weathering of old OM in rocks, remobilization of organic matter from thawing permafrost, chemoautotrophy, as well as secondary production by microbes and animals contribute to the global organic matter pool (Eglinton and Repeta 2004; Middelburg 2011). Approximately two-thirds of the terrestrially produced OM is rapidly degraded within soils or glacial environments. The remainder escapes immediate degradation and is either degraded slowly or temporarily stored before being transported downstream with old, weathered OM into lakes, streams, rivers, coastal transition zones and, ultimately, the ocean (Regnier et al. 2013). An estimated 1.9 Pg C year−1 ± 1.0 Pg C year−1 of total soil C (mostly particulate OM and dissolved OM, but also dissolved inorganic carbon) is exported to inland waters. Only 0.45 Pg C year−1 of the terrestrial derived OM reaches the coastal ocean and 0.1–0.35 Pg C year−1 makes it to the open ocean (Regnier et al. 2013; Bauer et al. 2013). Thus, the intermittent storage and transport of OM along the land-ocean continuum modulates the degradation of terrestrial OM on short and long timescales. However, the exact amounts of OM that are degraded and temporarily or permanently preserved during its transit from land to ocean remain unknown (Regnier et al. 2013). Like terrestrially derived OM, a large fraction of the OM produced in the surface ocean is rapidly degraded with only approximately 10–20% of the primarily produced OM (of which ca. 27% is dissolved OM) escaping degradation in the surface ocean (Dunne et al. 2007; Hansell and Carlson 2015). Dissolved organic matter, DOM , is transported to the deep ocean by convection and mixing. While a large fraction of the exported DOM is degraded at mid-depths, an estimated 0.1 Pg C year−1 is transfered to the large, apparently refractory, deep ocean DOM reservoir (~680 Pg) that persists through multiple ocean mixing cycles (Hansell and Carlson 2015). Particulate OM, POM , sinks to the ocean floor and can also be laterally transported by ocean currents (Eglinton and Repeta 2004). It is further degraded during its transport, resulting in an attenuation of the export flux. Between 0.28% and 30% (5.7% average) of the export flux reaches depths greater than 1.5 km and <1–5% of the export flux is deposited on the seafloor. Degradation during burial further reduces this flux such that <0.3% of the original exported flux is ultimately sequestered in deep sediment layers (Honjo et al. 2008; Dunne et al. 2007; Eglinton and Repeta 2004).

The Process of OM Degradation and Preservation

OM degradation and preservation are often thought of as two sides of the same coin. However, this view is somewhat simplistic. It is important to realize that OM preservation is not solely defined by the absence of degradation but can also be directly controlled by other factors, such as the addition of so-called necromass derived from remnants of bacterial cell walls, cell exudates, or cell lysis products to the sinking or buried OM pool. Nevertheless, OM degradation still exerts the dominant control on OM preservation, and many of the additional controls on preservation are indirectly linked to the process of OM degradation.

The degradation of OM generally proceeds via multiple enzymatic reactions involving millions of different organisms and organic compounds, as well as a number of different oxidants and intermediate compounds (Arndt et al. 2013). Note that although microbes dominate organic matter consumption, fungi, as well as animals, such as corals, sea sponges, and suspension feeders also consume detrital organic matter (Bianchi 2011; Middelburg 2017). A fraction of the consumed carbon is excreted as faeces or pseudofaeces, further contributing to the sedimentary pool.

OM Composition

The composition of OM , from freshly produced to heavily degraded, ranges in size and composition from simple, small monomers to large polymers and humic substances (de Leeuw and Largeau 1993). In the terrestrial biosphere, primary production is mainly carried out by multicellular plants, with litter, roots, and root-zone exudates that often contain rigid polymers such as cellulose and lignin, complex carbohydrates, or phenolic polymers for structural support (de Leeuw and Largeau 1993). In contrast, marine primary production is dominated by single celled organisms and, therefore, rich in lipids and nitrogenous compounds (Burdige 2007; Arndt et al. 2013). All these compounds are present in the environment at various stages of degradation from unprocessed and reactive to highly processed and less reactive OM. In addition, it has also been suggested that, despite its low contribution compared to primary production, secondary production by microbes and animals might exert an important control on the composition of sedimentary organic matter that is eventually buried (Lomstein et al. 2012; Middelburg 2017).

Microbes and Terminal Electron Acceptors

This heterogeneous mix of organic compounds is mainly degraded by millions of individual microorganisms with highly diverse metabolic potentials and requirements in synergetic or competitive interactions (Jørgensen and Marshall 2016; Jørgensen and Boetius 2007; Jørgensen 2006). They can use different oxidants (i.e., terminal electron acceptors, TEAs , O2, NO3 , Mn(VI), Fe(III), and SO4 2−) to degrade OM and produce a number of intermediate organic compounds. Although some microorganisms can take up OM directly, most rely on the production of extracellular hydrolytic enzymes in order to make large organic compounds accessible to the entire community. Fermenters, in turn, are then often required to convert these smaller organic compounds into substrates that can be used by other heterotrophs. Consequently, an interconnected group of microorganisms is often required to break down organic matter into terminal products such as CO2, H2, and CH4. Depending on the degradation pathway, OM is thus directly oxidized to CO2, partly oxidized to intermediate compounds or reduced to CH4. The main sequence of these different degradation pathways roughly follows the decreasing amount of energy available from them.

Controls on OM Degradation and Preservation

Although OM degradation and preservation are intimately linked, the relative significance of different mechanisms in controlling OM degradation versus preservation may vary (Burdige 2007). The reason for this difference is the low preservation efficiency of OM in the Earth system. Ultimately, only a tiny fraction of the photosynthetically produced OM is preserved in the sediment and small changes in degradation rates translate into pronounced changes in preservation rates. It is therefore important to keep in mind that a mechanism that exerts only a subtle control on OM degradation may play an import role for OM preservation.

In general, OM degradation and preservation rates are controlled by a dynamic and complex interplay of different environmental factors that can be broadly divided into quantity and quality controls (Figure 1).
Figure 1

The degradation and preservation of organic matter (OM) is controlled by the quantity and quality of organic matter (Adapted from Arndt et al. 2013). The organic matter supply to an environment can be donor or consumer controlled and its degradation and preservation in this environment is thermodynamically and/or kinetically controlled through the different physiological abilities of the resident microbial community that compete for common substrates. In addition, transport processes exert an indirect control through their influence on organic matter alteration (and thus composition), terminal electron acceptor (TEA), metabolic intermediate concentrations, and microbial community structure.

Quantity Control

OM degradation and preservation are first and foremost determined by the quantity of available carbon. In this respect, one can distinguish consumer- and donor-controlled systems (Arndt et al. 2013; Middelburg 2017). Consumer-controlled systems, such as the surface soil layer and the photic layers of aquatic systems and sediments have a control over carbon delivery by enhancing OM production or transport, while donor-controlled systems, such as deep soil layers, the deep ocean, and marine sediments outside of the photic zone, have little or no control over C input. In those systems, organic matter degradation is closely linked to organic matter export efficiencies . For instance, a higher vertical transport rate increases the deposition flux of OM to marine sediments and reduces the degree of alteration and thus the aging of organic matter in the water column.

Quality Control

Organic matter quality (i.e., its susceptibility to microbial transformation or reactivity ) exerts an important influence on rates of OM degradation and preservation. The historic view is that OM quality is primarily determined by its chemical structure. However, it has become increasingly clear that OM quality is “not an inherent, or absolute, property of the organic matter itself, but results from the interaction between the organic matter and its environment” (Mayer 1995). Recent observations and laboratory experiments indicate that OM quality is controlled by a complex and dynamic interplay between OM structure and numerous environmental factors (e.g., Schmidt et al. 2011; Burd et al. 2016). The source and transit path of OM, its composition, the nature of the resident microbial community, temperature, physical protection, macrofaunal activity, deposition rate, and thermodynamic constraints all are thought to influence rates of OM degradation (Arndt et al. 2013; Burd et al. 2016), which vary by at least 10 orders of magnitude (Middelburg 1989).

OM Composition

One of the most important guideposts to understanding the link between OM composition and OM quality is the recognition that terrestrial OM is generally less reactive than marine OM (Burdige 2007). This quality difference has been explained with differences in the chemical structures between terrestrial OM, which is made up of moderately or highly resistant biopolymers, and marine OM, dominated by comparably labile biopolymers (de Leeuw and Largeau 1993). In addition to its original chemical composition, the continuous alteration of OM during transport and burial influences the quality of the residual OM. Observations show a pronounced decrease of OM quality with time (Middelburg 1989). This observation has been explained with preferential degradation of more reactive OM compounds during OM degradation. A continuous degradation of OM during transport and burial will thus result in the selective preservation of unreactive compounds and an overall decrease in OM quality (Tegelaar et al. 1989). In addition, the formation of geopolymers through humification or condensation–polymerization during transport and, especially, burial also contributes to the overall decrease of OM quality with time (Tissot and Welte 1984; Burdige 2007).

Microbial Community Structure

Because a vast array of microorganisms consumes, produces, and transforms organic compounds, the microbial community structure exerts an important control on apparent OM quality. Unlike macrofauna, microorganisms can be dispersed over vast distances in short time spans, have the ability to use different electron donors and acceptors (within one organism), can achieve dormancy, can respond rapidly to shifting environmental variables, and can evolve and exchange genetic material with distantly related organisms much faster than their macroscopic counterparts (Nemergut et al. 2013). The rate at which these organisms are active depends on their access to energy and nutrients, their inherent metabolic capabilities, and the presence and/or absence of other microorganisms and viruses that carry out ecological functions such as predation and vitamin, antibiotic and extracellular enzyme production (Lever et al. 2015; Jørgensen and Marshall 2016). For instance, it has long been thought that most bacteria cannot ingest organic compounds larger than ~600 g/mol (Decad and Nikaido 1976), but many of the organic compounds that reach sediments are larger than this (e.g., proteins, nucleic acids, lipids). Aerobic organisms have the ability to oxidize organic matter compounds directly to CO2 but are confined to the usually thin oxic zone (few mm to a cm deep, although it can extend to 100s of meters in the organic lean ocean gyres). In contrast, the anaerobic food chain usually requires an initial hydrolytic step to break down high molecular weight compounds through extracellular and membrane-bound enzymes into smaller organic molecules such as monomeric sugars and amino acids. These hydrolytic products can then be oxidized by microorganisms to CO2 or transformed by fermenting and acetogenic bacteria to hydrogen and organics such as volatile organic acids. The terminal step in this anaerobic food chain involves the utilization of these latter compounds by microorganisms that reduce manganese/iron oxides, sulfate, or produce methane. In addition, newly discovered physiologies, such as extracellular electron transfer for remote oxidation of OM by cable bacteria (Nielsen et al. 2010), may require revision of the traditional view of OM degradation pathways.

Thermodynamics

Most of the organic matter that is consumed by microorganisms is used to gain energy. Although there are many factors that govern the rates at which organisms will consume energy, there is a growing consensus that the rates at which catabolic reactions proceed in relatively low-energy settings are related to the amount of energy that is available from them (Jin and Bethke 2003; LaRowe et al. 2012). In other words, the rate of OM degradation slows down as the amount of Gibbs energy available from it decreases. The Gibbs energy yield of organic matter degradation is determined by the nature of the available terminal electron acceptor, the organic compounds being processed, and the end products of the decomposition reaction, as well as temperature, pressure, and the chemical composition of the environment (LaRowe and Van Cappellen 2011). For instance, OM degradation rates in anaerobic sediments in which the dominant electron acceptor is sulfate tend to be slower than in oxic settings. When only organic carbon compounds with a low energetic potential remain, reaction rates can slow even further.

Physical Protection

The observed correlation between the content of organic matter in soils and sediments and mineral surface area indicates that physical protection of organic matter by interactions with the mineral matrix exerts an important control on OM degradation and, in particular, preservation (Mayer 1994; Hedges and Keil 1995; Blair and Aller 2012). Sorption of organic matter to mineral surfaces or its inclusion in aggregates provides means of protecting reactive organic matter from degradation during transport and burial and, thus, favors preservation. Multiple mechanisms, such as the protection from or steric limitations of hydrolytic enzyme attack and condensation reactions (Mayer 1994; Hedges and Keil 1995; Eglinton and Repeat 2004) have been proposed to explain the observed physical protection of organic matter by minerals, although this remains the subject of much debate .

Temperature

Like all other biogeochemical processes, temperature is a master variable that generally speeds up reaction rate as it rises. However, organic matter degradation is not a simple chemical reaction, but a complex, multi-step process involving a number of different OM compounds, enzymes, oxidants, and intermediate products. As a consequence, the control of temperature on organic matter degradation rates also depends on physiological adaption, selection pressure, and the reaction path (Arnosti et al. 1998; Finke and Jørgensen 2008; Robador et al. 2010). For instance, organic matter degradation rates in temperate environments strongly increase during the warm season and fall during cooler months. In contrast, organic matter degradation rates in permanently cold Arctic sediments are not necessarily slower than those in temperate or tropical environments (Jørgensen 2006). This seemingly contradictory observation is the direct result of the physiological adaption of the in-situ bacterial community to the prevailing environmental conditions.

Transport Processes

Transport processes, such as bioturbation , bioirrigation, and deposition rates may exert an important direct and/or indirect control on organic matter degradation and preservation (Middelburg 2017). In soils and oxic sediments, invertebrates such as polychaetes rework the upper centimeters and influence degradation rates through feeding and burrowing activities, the ventilation of these burrows, or mixing of fresher organic material to deeper layers. This activity may enhance or inhibit organic matter degradation. For instance, within the bioturbated zone of oxic sediments, short-term redox oscillations, the mixing of fresh and labile with old and degraded OM (so-called priming ), bioturbation-mediated particle manipulation, grazing, and excretion/secretion may enhance degradation rates, while the production of tube linings, halophenols, or body structural products and the direct feeding on depositing organic matter could inhibit organic matter degradation (Arndt et al. 2013; Middelburg 2017). In addition, the interaction between different macrobenthic animals may enhance the supply of organic matter to the sediment.

Finally, in marine sediments, organic matter degradation and preservation often correlate with sediment deposition rates. However, deposition rate only exerts a control on organic matter degradation/preservation if deposition rates are high enough and/or the organic matter is unreactive enough to escape degradation in the upper, mixed layer (Emerson et al. 1985). One can broadly distinguish different high deposition settings (Blair and Aller 2012). High-energy, mobile muds generally reveal high organic matter degradation and low preservation due to enhanced oxygen exposure and efficient metabolite exchange. Low-energy facies show low organic matter degradation rates and enhanced organic matter preservation as a result of extreme accumulation rates and, often, high loads of fossil organic carbon. Small, mountainous river systems exhibit the highest organic matter preservation favored by the delivery of large amounts of fossil organic matter and average, but periodically high, accumulation rates.

Summary

Organic matter degradation and preservation play a key role in global biogeochemical cycles and climate. The degradation of OM generally proceeds via multiple enzymatic reactions involving millions of different organisms, billions of organic compounds, and a number of different oxidants, as well as intermediate compounds. As a result, OM degradation and preservation is controlled by a dynamic and complex interplay of different environmental factors. Attempts to isolate the impact of a single variable on the rate of OM degradation have often led to contradictory results. It is therefore becoming increasingly clear that OM degradability is not an intrinsic property of the organic matter itself but an ecosystem property. Correspondingly, the likelihood that a given organic compound will be degraded by a microbial community or be preserved will depend on the chemical formula and structure of that compound, in addition to the metabolic capabilities of the resident microorganisms in response to environmental factors such as electron acceptor and intermediate metabolite concentrations, temperature, and physical associations with minerals or other organic compounds.

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Authors and Affiliations

  1. 1.BGeosys, Department Geoscience, Environment & Society (DGES)Université Libre de BruxellesBruxellesBelgium
  2. 2.Department of Earth SciencesUniversity of Southern CaliforniaLos AngelesUSA