[Advances in Marine Biology] Aquatic Geomicrobiology Volume 48 || Heterotrophic Carbon Metabolism

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  • 3. Aerobic Carbon Oxidation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 144

    4.2. Anaerobic respiration . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 150

    4.3. Partitioning of total benthic metabolism into respiration pathways . . . . . . . . . . . . . 152

    5. Carbon Assimilation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 155

    carbon inventory on Earth (0.002%) and of the active carbon pool (2%)

    represented by unaged dead organic matter, dissolved organic carbon, inor-from limestone enters the atmosphere as CO2 or enters aquatic environments

    mostly as HCO3 . Atmospheric CO2 tends to equilibrate with the carbonatesystem of the oceans (Takahashi et al., 1997; Fasham et al., 2001),ganic carbon, and atmospheric CO2 (Hedges and Keil, 1995). Numerous

    transformation modes and pathways deliver carbon to the diVerent pools(Table 5.2). Inorganic carbon oxidized from organic matter or weathered6. Degradability and Decomposition Kinetics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 159

    7. Carbon Preservation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 162

    1. INTRODUCTION

    Carbon is central to all life, and it is the most actively cycled element in the

    biosphere. Most carbon is tied up as inorganic carbon in limestone or

    in fossil organic pools such as bitumen and kerogen in shales (Table 5.1).

    The carbon in living biomass represents only a small fraction of the total4. Anaerobic Carbon Oxidation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 147

    4.1. Hydrolysis/fermentation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 148Chapter 5

    Heterotrophic Carbon Metabolism

    1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 129

    2. The Detritus Food Chain. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 132

    2.1. The chemical nature of detritus. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 132

    2.2. Organisms decomposing detritus. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 134

    2.3. Detritus and dissolved organic matter (DOM). . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 137and therefore, these two carbon pools are coupled. Inorganic carbon enters

    living biomass (LPOC [living particulate organic carbon]) via carbon fixa-

    tion by autotrophic organisms (e.g., plants and algae; see Chapter 4).

    ADVANCES IN MARINE BIOLOGY VOL 48 2005 Elsevier Inc.0-12-026147-2 All rights reserved

  • 130 CANFIELD ET AL.Table 5.2 Major transformations of carbon in the lithosphere

    Table 5.1 Major carbon reservoirs on Earth

    Type of pool LocationPool size(g C)

    CO2 gas Atmosphere 6.6 1017Living biomass (LPOC) Aquatic and terrestrial 9.5 1017Dissolved organics (DOC) Aquatic 1.5 1018Dead organics (DPOC) Sediments and soils 3.5 1018Dissolved CO2 Aquatic 3.8 1019Carbonates (CaCO3, Mg(CO3)2) Carbonaceous rock 6.0 1022Fossil organics Sedimentary rocks 1.5 1022

    From Bowen (1979); Hedges and Keil (1995).Decomposing biomass is converted back to inorganic carbon through

    hydrolysis/fermentation (dissolved organic carbon [DOC] formation) and

    subsequent mineralization (CO2 formation) by heterotrophic organisms

    (Canfield, 1993; Kristensen and Holmer, 2001).

    Not all the dead particulate organic carbon (DPOC) in sediments and soils

    is available for biological decomposition, either because of a refractory

    chemical structure or because environmental conditions are unfavorable

    for microbial activity. The carbon escaping mineralization will be buried

    permanently in deep sediments and soils, and after enough time (millions of

    years), it will end up as fossil organics in sedimentary rock, fossil hydro-

    carbons, and natural gas. On long time scales, fossil carbon is returned to the

    Earths surface for subsequent oxidation. The human circumvention of this

    natural carbon cycle through the burning of coal and other fossil fuels is well

    known; it currently increases the atmospheric concentration of CO2 about

    0.5% per year, bringing present CO2 levels to 34% above their pre-industrial

    average value (DuVy et al., 2001; Soon et al., 2001).

    Pathway Transport mechanism

    Atmospheric CO2 ! Oceanic HCO3 DiVusive transportInorganic C (CO2, HCO

    3 ) ! Organic C Photo- and chemolithoautotrophy

    Inorganic C (CO2, HCO3 ) ! Carbonates Precipitation, mostly biological

    Organic C ! Inorganic C (CO2, HCO3 ) Decomposition, mineralizationFresh organic C ! Fossil C Sedimentation and burial with timeFossil C ! Atmospheric CO2 Human combustion of fossil fuels

  • Microorganisms grow and divide, and this requires energy, nutrients, and

    often organic building blocks from the environment. As outlined in Chapter

    3, energy-gaining activities are referred to as catabolic (dissimilatory or

    energy) metabolism, whereas the synthesis of cellular material is referred to

    as anabolic (assimilatory) metabolism. These two types of metabolism are

    coupled in the sense that microorganisms use a large share of the energy

    gained during catabolism to fuel anabolic carbon assimilation (Table 5.3).

    A variety of terms describe catabolic processes, including fermentation,

    respiration, decomposition, degradation, decay, and mineralization. Fer-

    mentation, as we saw in Chapter 3, occurs when organic matter acts as

    both the electron acceptor and the electron donor in organic matter break-

    down. Decomposition, degradation, and decay are three similar terms de-

    scribing the overall enzymatic processes mediating (1) the dissolution of

    particulate organic polymers into large macromolecules (hydrolysis),

    HETEROTROPHIC CARBON METABOLISM 131(2) the cleavage of these into smaller moieties (fermentation), and (3) the

    terminal oxidation (respiration) of the organic carbon by various electron

    acceptors, such as oxygen, manganese oxides, nitrate, iron oxides, and

    sulfate (Table 5.4). More generally, respiration refers to all catabolic reac-

    tions generating ATP involving both organic and inorganic primary electron

    donors and electron acceptors, including, therefore, also chemolithoauto-

    trophic and chemolithoheterotrophic processes (see also Chapter 4). The

    term mineralization refers to the terminal oxidation of organic carbon into

    inorganic (mineral) form.

    Aerobic and anaerobic heterotrophic microorganisms are responsible for

    a large proportion of the organic carbon oxidation occurring in aquatic

    environments. This Chapter focuses on these heterotrophic processes of

    carbon mineralization. We look at the relationship between microbial acti-

    vity and carbon source and consider the role of microorganisms in the

    Table 5.3 ATP use for a microbial cell grown onglucose

    ProcessAvailableATP (%)

    SynthesisPolysaccharides 6.5Protein 61.1Lipid 0.4Nucleic acids 13.5

    Transport mechanisms 18.3

    From Fenchel et al. (1998).

  • leading to the preservation of organic carbon in sediments. This Chapter is

    a springboard to subsequent Chapters, which discuss the specifics of

    132 CANFIELD ET AL.individual elemental cycling by microbes.

    2. THE DETRITUS FOOD CHAINdetritus food chain. We also outline the various pathways of both aerobic

    and anaerobic organic carbon mineralization, and we consider the processesTable 5.4 Schematic overview of chemotrophic catabolic (dissimilative) pro-cesses mediated by microorganisms

    e acceptor

    e donor

    H2 CH2O CH4 HS NH4 N2 NO2 Fe

    2

    CH2O 1 1 CO2 2 2 SO24 3 3 3 Fe3 4 4 4 9 NO3 5 5 5 9 11 Mn4 6 6 6 9 12 O2 7 7 7 9 10 10 8

    1, fermentation; 2, methanogenesis; 3, sulfate reduction; 4, iron reduction; 5, denitrification;

    6, manganese reduction; 7, aerobic respiration; 8, iron oxidation; 9, sulfide oxidation;

    10, nitrification; 11, anammox; 12, anoxic nitrification.2.1. The chemical nature of detritus

    In many ecosystems a significant part of the organic production is not

    consumed or assimilated by animals but is instead converted to the pool of

    dead organic matterthe detritus pool (Figure 5.1) (see Wetzel et al., 1972).

    The fraction of primary production entering the detritus pool as particulate

    and dissolved organic matter is highly dependent on the composition of the

    plant community. Phytoplankton is the predominant detritus source in

    the open ocean and deep lakes, whereas macroalgae and vascular plants

    are more important in coastal marine areas, shallow lakes, and rivers. The

    chemical composition of plants and algae is well defined, and 90100% of

    the organic matter consists of carbohydrates (cellulose, alginate), proteins,

    lipids, and lignin (Table 5.5). Lignin is only present in significant amounts in

    terrestrial vascular plants (1030%), whereas phytoplankton may contain

    more than 50% protein (Hodson et al., 1984; Hedges et al., 2002). Animal

  • HETEROTROPHIC CARBON METABOLISM 133tissues, on the other hand, are very rich in protein (up to 80%; Kristensen,

    Figure 5.1 Fate of organic production by primary producers, in this case,seaweed. The plant biomass will either be grazed by herbivores or enter thefood chain as dead organic matter. Plant remains enter the detritus pool togetherwith herbivore feces and carcasses. Detritus is either decomposed by microorganismsor consumed by detritivores together with microorganisms. Finally, the detritivorefeces (and carcasses) return to the detritus pool together with carnivore remains, ifpresent.1990). Prokaryotes contain about 50% protein, and together with carbohy-

    drates and lipids, about 80% of prokaryote biomass can be accounted for

    (Madigan et al., 2003). The remainder is composed of nucleic acids and cell

    wall constituents (murein, teichoic acid, and lipopolysaccharide).

    In total, detritus consists of ungrazed plant material, along with macro-

    faunal feces, carcasses, exuviae, and dead microbial cells. The fraction of

    recognizable biochemical constituents decreases as detritus passes through

    the food chain. In the eastern and equatorial Pacific, for example, the chemi-

    cal composition of living phytoplankton and zooplankton is well character-

    ized (>80%, Table 5.5). However, only about 3060% of the organicmatter can be characterized in the flocculent layer at the sediment surface

    at depths of 3500 to 4000 m, and this decreases to 20% or less at 10 cm depth

    in the sediment (Wakeham et al., 1997; Wang et al., 1998). The largely

    uncharacterized and relatively refractory organic carbon fraction was once

    thought to be formed by spontaneous polycondensation reactions among

    small reactive intermediates released during the enzymatic breakdown of

    biomolecules, forming, in some cases, highly refractory geopolymers.

    Evidence suggests, however, that this uncharacterized fraction probably

    has more complex formation pathways than previously recognized (Hedges

    et al., 2000).

  • 134 CANFIELD ET AL.Table 5.5 Carbohydrate, lignin, lipid, and protein content as percentage of totalorganic matter in (A) selected plants, animals, and microorganisms (adapted fromKristensen, 1990), and (B) phytoplankton, zooplankton, the top 24mm looseflocculent layer of sediment (sediment floc), the upper cm of the sediment, and the1014 cm depth interval of sediment at 4100 m depth in the eastern Pacific (fromWang et al., 1998)

    Material Carbohydrate Lignin Lipid Protein

    (A)Chlorella sp. 33.4 0 16.1 46.4 95.9Skeletonema costatum 32.5 0 7.3 57.8 97.6Ulva lactuca 77.0 0 0.1 22.7 99.8Fucus vesiculosus 90.7 0 2.6 6.6 99.9Aquatic angiosperm 81.5 0 2.1 16.1 99.7Barley straw 82.6 13.6 1.0 1.0 98.2Tree-leaves 77.1 12.5 2.9 6.7 99.2Pine wood 71.7 26.7 1.5 0 99.9Polychaete worm 4.8 0 9.0 78.5 92.3Bivalve 20.0 0 4.0 71.1 95.1Prokaryote 16.6 0 9.4 52.4 78.72.2. Organisms decomposing detritus

    Microorganisms play a dominant role in the breakdown of detritus, for

    which there are several reasons. First, microbes can hydrolyze a diverse

    assemblage of organic compounds, some of which are totally indigestible

    by animals. Second, due to their small size and consequently large surface-

    to-volume ratio, they have the ability to take up and utilize carbon sources

    and mineral nutrients eYciently in dilute solutions (see Chapter 2). Further-more, small cells can create intimate contact with solid surfaces and thus

    minimize loss of products from exoenzyme activity. Finally, microbes can

    maintain an eYcient metabolism and mineralize organic substrates underanoxic conditions. Prokaryotes are important decomposers of detritus in

    most aquatic environments, but fungi may contribute significantly in certain

    environments, particularly in freshwater settings. Thus, fungi can account

    for up to 96% of the microbial biomass associated with vascular plant litter

    entering lakes and rivers (Baldy et al., 1995). By contrast, in seagrass beds

    and salt marshes fungi usually account for no more than 20% of the total

    microbial biomass associated with litter, whereas values as high as 80% have

    (B)Phytoplankton 48 0 19 24 91Zooplankton 14 0 39 46 99Sediment floc 19 0 3 35 5701 cm sediment 16 0 3 17 361014 cm sediment 5 0 2 11 18

  • been recorded from mangrove forests (Blum et al., 1988). The role of fungi is

    reduced even further in anoxic sediments, particularly if the sediments are

    sulfidic (Mansfield and Barlocher, 1993).

    The amount of primary production consumed by herbivorous animals in

    aquatic environments is positively correlated with the nutrient (i.e., protein)

    content of the primary producer, and it is inversely correlated with the

    primary producer C:N ratio (Table 5.6). Animals, having a C:N ratio of

    46, require a diet with a C:N ratio below about 17 (Russell-Hunter, 1970).

    Thus, the high C:N ratio and the high content of structural carbohydrates

    (cellulose and hemicellulose) associated with lignin in vascular plants, and

    for certain polysaccharides in macroalgae, restricts the herbivory of these

    plant types. It is not surprising, then, that most animals lack digestive

    enzymes for hydrolyzing structural plant components and that only a few

    aquatic animals are capable of utilizing the tissues of vascular plants. Phy-

    toplankton and benthic microalgae, on the other hand, are readily grazed

    HETEROTROPHIC CARBON METABOLISM 135and digested by zooplankton and benthic animals.

    Many herbivores feed on a variety of substrates, both living and dead, in

    order to balance their nutrition. For example, the grapsid crab Sesarma messa

    can process 3070% of the total leaf production in certain mangrove forests

    by eating both attached leaves and fallen leaf litter (Robertson et al., 1992).

    Because leaves from mangrove trees are poor in nut...

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