SCOPE 21 -The Major Biogeochemical Cycles and Their Interactions  

ABSTRACT

The bacterial reductions and oxidations of sulphur compounds have an auxiliary function in the transformation of inorganic to organic carbon. Sulphate acts as an additional electron acceptor when free oxygen is consumed. In this capacity, sulphate is quantitatively more important in the marine environment than nitrate or bicarbonate. A number of new genera of sulphate and sulphur reducing bacteria have been described recently. In addition, the variety of organic compounds used in the dissimilatory turn-over of inorganic sulphur was found to be less restricted than formerly assumed. In the flow of energy, the oxidation of hydrogen sulphide by chemosynthetic bacteria must be considered as a form of secondary production. In the marine environment obligately chemo-autotrophic, acid-producing sulphur oxidizers are less prevalent than facultatively chemoantotrophic, base producing (polythionate) sulphur oxidizers. Anaerobic photosynthetic sulphide oxidation occurs effectively in estuaries only. On the global scale, the amount of chemosynthetic production is minimal as compared to photosynthetic production. Recently, however, symbiotic chemosynthesis has been found to sustain rich invertebrate populations clustered around sulphide emitting hydrothermal deep-sea vents.

19.1 INTRODUCTION 

The foreword to the 13th SCOPE Report (Bolin et al., 1979) states that the carbon cycle is `the pacemaker for the other cycles which in turn co-determine flow rates in the carbon cycle' and describes most closely the occurrence and intensity of life processes in the biosphere. It is of primary interest, then, how these other cycles, primarily those of nitrogen, phosphorous and sulphur, do interact with and aid the carbon cycle.

The marine environment, which, by volume, constitutes by far the largest portion of the biosphere, is specifically characterized by a strong involvement of sulphur transformations in the production and decomposition of organic carbon. This chapter outlines briefly the biogeochemical linkages between the carbon and sulphur cycles and their effect on the flow of energy within the food chain.

19.2 SULPHATE REDUCTION

Sea-water, as compared to fresh-water and most soils, contains relatively high contents of sulphur, primarily present in the form of sulphate. The assimilatory utilization of this sulphate for biosynthesis in plants and micro-organisms never becomes a growth limiting process nor does it lead to sulphate depletion in marine environments. The dissimilatory reduction of sulphate by bacteria (anaerobic respiration) on the other hand, plays a more conspicuous role. Here the sulphate functions as an additional electron sink available after the consumption of free oxygen. In this capacity it is of more quantitative importance than nitrate or carbon dioxide, the other possible electron acceptors (see Martens and Jannasch, comment to Chapter 18, this volume).

In Figure 19.1, bacterial sulphate reduction appears as anaerobic organic decomposition. It occurs in the interstitial water of organically rich marine sediments or in stagnant estuarine waters where the dissolved oxygen has been consumed by decomposition processes (aerobic respiration). This reduction of sulphate to hydrogen sulphide by specific groups of bacteria is quantitatively by far more important in marine environments than the deamination of organic sulphur compounds (i.e. the release of HS from S-containing amino acids) during degradation processes. Deuser (1970) estimated, on the basis of ¹³C determinations and the atomic ratio of sulphur to carbon in marine organic matter, that 95 to 97% of the sulphides in the Black Sea originate from bacterial sulphate reduction, the rest by decomposition of organic sulphur-containing compounds.

The hydrogen sulphide formed may escape immediate biological or chemical oxidation in stagnant waters which, in the marine environment, are limited to a few large oceanic water bodies like the Black Sea (Degens and Ross, 1974) and the Cariaco Trench (Richards, 1975) and to small nearshore pockets such as certain Norwegian and British Columbian fjords (Richards, 1965). These waters are permanently anoxic and the O₂H₂S interface is located in the water column usually, but not always, below the reach of sunlight. Hydrogen sulphide has a stabilizing effect on oxic-anoxic interfaces; its reactivity with metals enhances the chemical stratification (Brewer and Spencer, 1974).

Figure 19.1 Scheme of the auxiliary nature of the sulphur cycle within the various stages of the carbon cycle and the types of microbial transformations. The assimilatory reduction of sulphate to organic sulphur compounds and release of hydrogen sulphide by deamination are not included. They play a minor role in the marine environment. Primary photosynthetic production (photosystem II) or organic carbon is indicated by the solid square. The dashed square represents secondary chemosynthetic production (including some primary bacterial production by photosystem I)

At the present time, our knowledge of the microbiology of sulphate reduction is rapidly expanding. Five new genera of sulphate reducing bacteria have recently been isolated (Widdel and Pfennig, 1977, 1981a, b; Widdel, 1980).

19.3 SULPHUR OXIDATION 

The reduced sulphur compounds, mainly hydrogen sulphide, can serve, in turn, as sources of electrons for bacterial chemosynthesis. As in photosynthesis, inorganic carbon is reduced to organic carbon while, however, the oxidation of sulphur serves as the source of energy instead of light. This oxidation may go all the way to sulphate by acid producing sulphur bacteria or may stop at an intermediate oxidation state. One of the latter cases, the production of polythionates, has often been found in the marine environment and results in a slight increase in pH (Tuttle and Jannasch, 1973, 1979). The chemosynthetic sulphur oxidizing bacteria cover a large variety of morphological and physiological types. Many of them are facultative sulphur oxidizers that may also derive their energy for growth from the oxidation of organic compounds. This appears to be a common microbial behaviour in the marine environment where, due to the powerful buffering capacity of the CO₃²/HCO₃ system, acidophilic and obligately sulphur oxidizing bacteria are not able to produce a pH low enough for a successful competition with the non-acidophilic bacteria (Tuttle and Jannasch, 1973).

Since hydrogen sulphide is a product of sulphate reduction that, in turn, uses photosynthetically produced organic matter as reductant, chemosynthesis by sulphur oxidizing bacteria must be considered in the flow of energy as a form of secondary production. In Figure 19.1 the microbial sulphur oxidation appears twice: as the aerobic and chemosynthetic process and as an anaerobic photosynthetic process. Bacterial anaerobic reduction of CO₂ requires light as a source of energy and uses hydrogen sulphide solely as a source of electrons. Therefore, if the above terminology is used, bacterial photosynthesis represents, as does green plant photosynthesis, a form of primary production. This distinction between primary and secondary production of organic carbon is important if the interactions between the carbon and sulphur cycle are linked to the flow of energy, be it light or chemical energy. This is well illustrated in the case of the hydrothermal vent processes discussed below.

Chemosynthetic sulphur oxidation occurs primarily in shallow and highly productive marine waters, such as estuaries and lagoons, and the H₂S/O₂ interfaces between the above mentioned anoxic marine basins and the overlying waters. A special case is the H₂S and Thioploca-containing microbial mats found 50 to 280 metres deep off the Chilean and Peruvian coast (Gallardo, 1977). In general, however, the total amount of organic carbon produced by bacterial chemosynthesis is minute if contrasted with that generated by green plant photosynthesis. This is mainly due (1) to the relatively small amount of energy available in the form of H₂S in contrast to that of light and (2) to the lower biochemical efficiency of chemosynthesis as compared to photosynthesis with respect to CO₂-reduction. Yet, chemosynthesis might be of local importance (Kepkay et al., 1979) especially in the absence of light (Tuttle and Jannasch, 1979). Chemosynthesis based on the bacterial oxidation of hydrogen, ammonia, nitrite, iron, and possibly manganese may occur in marine and non-marine environments alike. However, when calculated from the sheer amounts of reduced sulphur compounds contained in anoxic sea-water and marine sediments, sulphur-based chemosynthesis must be assumed to be prevalent, relative to these other electron donors in the marine environment.

Green plant photosynthesis uses H₂O rather than H₂S for the electron source and, except for some assimilatory sulphate reduction, is not involved in the direct interaction between the sulphur and carbon cycles as shown in Figure 19.1. The other two important transformations of carbon, aerobic decomposition and anaerobic fermentation, involve the breakdown of organic sulphur compounds to incompletely oxidized intermediates or to inorganic sulphides. These transformations are not linked to the dissimilatory and quantitatively major portion of the sulphur cycle. Relatively small amounts of the volatile dimethylsulphide are produced by phytoplankton and emanate into the atmosphere (Andrea, 1981); while deposition and burial of metal sulphides and disulphides in anoxic marine sediments are substantial (a review of the S cycle is given in Chapter 2, this volume).

Figure 19.2 Scheme of a short-cut microbial sulphur cycle according to Pfennig and Biebl (1976). Ethanol and propanol may also be used by such syntrophic mixed cultures of green sulphur bacteria with species of Desulphuromonas

Recently a short-cut sulphur/carbon cycle was described that explains the rare occurrence of large accumulations of elemental sulphur in marine anoxic environments. Elemental sulphur is commonly produced in considerable quantities intra- and extracellularly by chemosynthetic as well as photosynthetic sulphur bacteria. There was, until recently, no microbial process known to oxidize or reduce elemental sulphur anaerobically. In a culture of Chlorobium, a green photosynthetic sulphur bacterium, Pfennig and Biebl (1976) discovered a new type of a sulphur reducing bacterium (Desulfuromonas acetoxidans) that oxidized acetate concomitantly (Figure 19.2). A syntrophic mixed culture of these two organisms in a closed bottle will cycle carbon and sulphur indefinitely as long as light is available as the source of energy. The new morphological and physiological types of sulphate and sulphur reducing bacteria described by Widdel (1980) and Widdel and Pfennig (1977, 1981a, b) are apt to change our notion of the microbial sulphur cycle substantially. Elemental sulphur can either be oxidized or reduced by a number of newly isolated organisms, and a much larger variety of organic substrates can be used for the reduction of sulphate than formerly anticipated. Beggiatoa, a sulphide oxidizing bacterium found abundantly in marshes and estuaries, has now also been shown to be capable of reducing elemental sulphur under certain conditions (Nelson and Castenholz, 1981).

19.4 HYDROTHERMAL VENTS

The recent discovery of hydrothermal vents of volcanic origin at tectonic ocean spreading centres at depths of 2500 to 2600 metres (Corliss et al., 1979) lends a new significance to bacterial chemosynthesis (Jannasch and Wirsen, 1979). Since the hydrogen sulphide contained in the emitted waters at concentrations of about 160 µM (Edmond et al., 1979) is of geothermic origin and not linked to photosynthetic primary production, the chemosynthetic conversion of inorganic to organic carbon at the vents must also be considered primary production. This terminology is based on hydrogen sulphide oxidation as the energy generating process and disregards free oxygen as the necessary electron sink, although it is a product of green plant photosynthesis.

During the percolation of sea-water through the earth's crust (Lister, 1977; Mottl et al., 1979), sulphate is reduced at temperatures of up to 500 °C and at high pressures. Thus, the source of energy for bacterial chemosynthesis in the deep sea is terrestrial rather than solar. Since no light is available, free oxygen, which is contained in deep sea waters at values above half atmospheric saturation, is required. It has been reported (Corliss et al., 1979; Mottl et al., 1979) that deep-sea-water penetrates into the porous lava layers and mixes with the highly reduced vent-water prior to emission. Thus, bacterial chemosynthesis appears to occur also in sub-surface lava cracks as evident from the high content of bacterial cells in the emitted waters of some vents (Karl et al., 1980).

The major reason for the absence of appreciable chemosynthetic production of organic carbon in basically similar hot springs located in shallow water or on land is the fact that light and atmospheric oxygen meet the highly reduced waters essentially at the same time. As a result of the overabundance of light energy versus the chemical energy available, photosynthesis surpasses chemosynthesis by far.

The high amount of chemosynthetically produced organic carbon and its suitability and availability as a food source at the deep-sea vents evidently result in the thriving populations of invertebrates clustered densely around the vent openings. At the present stage of our knowledge, there are three sites where reduced sulphur is aerobically oxidized with the concomitant production of organic carbon in the form of microbial biomass: (1) within the vents proper (Jannasch and Wirsen, 1979; Karl et al., 1980; Ruby et al., 1981); (2) within bacterial mats covering surfaces intermittently exposed to sulphide and oxygen contain sea-water in the immediate vicinity of the vents (Jannasch and Wirsen, 1981); and (3) within the invertebrates themselves in various symbiotic associations with chemosynthetic bacteria (Cavanaugh et al., 1981).

The latter represents a hitherto unknown phenomenon that appears to involve an evolutionary line from filter feeding bivalves to gutless vestimentiferan tube-worms. On the gill surface of the newly described clam Calyptogena magnifica (Boss and Turner, 1980) procaryotic cells seem to grow on as well as within the gill tissue. These unusually big clams live near the vents, where the water contains low levels of hydrogen sulphide. In the newly described pogonophore Riftia pachyptila (Jones, 1981) the entire ingestive and digestive intestinal tract appears to be replaced by a procaryotic tissue, the trophosome, which shows high activity of ribulose-diphosphate carboxylase, the enzyme characteristic for the reduction of carbon dioxide. The same is true for the clams' gill tissue. It is of great import that this entirely new principle of a direct interaction between the sulphur and carbon cycles within animals by exo- or endosymbiosis, or by both, appears to occur also in bivalves long known to inhabit marine anoxic and sulphide containing sediments of nearshore waters (Cavanaugh et al., 1981).

The total contribution of geothermal energy to oceanic primary production is minute as judged from the number of vents now known. The entire length of the ocean floor spreading belt around the globe is enormous, however, and if thousands or tens of thousands of vents do indeed exist, the terrestrial input of energy in the form of reduced sulphur or metals could be of consequence for the deep-sea food chain and abundance of fauna.

ACKNOWLEDGMENTS

This paper was prepared under support from the National Science Foundation Grants OCE79-19178 and OCE81-24253 and is Contribution No. 4921 from the Woods Hole Oceanographic Institution.

19.5 REFERENCES

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