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The Sulfur Cycle by Stefan M This article has This been published in or collective redistirbution of any portion of this article by photocopy machine, reposting, or other means is permitted only with the approval of The approval portionthe ofwith any permitted articleonly photocopy by is machine, of this reposting, means or collective or other redistirbution A S E A O F M I C RO B E S > SECTION IV. PROCEssES Oceanography > CHAPTER 9. MICROBES AND MAJOR ELEMENTAL CYCLES , V olume 20, The Sulfur Cycle N BY STEFAN M. SIEVERT, RONALD P. KIENE, AND HEIDE N. SchULZ-VOGT umber 2, a quarterly journal of journal The umber 2, a quarterly The ocean represents a major reservoir fur emissions have currently been over- reactions, called dissimilatory sulfur of sulfur on Earth, with large quanti- taken by anthropogenic emissions, pri- metabolism. These latter processes are ties in the form of dissolved sulfate and marily from the burning of fossil fuels. essential for the cycling of sulfur on our O ceanography Society. Copyright 2007 by The 2007 by Copyright Society. ceanography sedimentary minerals (e.g., gypsum Sulfur is an essential element for life. planet, and will be the primary subject and pyrite). Sulfur occurs in a variety However, at any given time, only a small of this article. of valence states, ranging from –2 (as fraction is bound in biomass. Sulfur Sulfur compounds can be used as in sulfide and reduced organic sulfur) makes up about 1% of the dry weight electron acceptors or electron donors in to +6 (as in sulfate). Sulfate is the most of organisms, where it occurs mainly as processes known as sulfate/sulfur reduc- stable form of sulfur on today’s oxic constituents of protein (primarily the tion and sulfur oxidation, respectively. Earth; weathering and leaching of rocks S-containing amino acids, cysteine and Whereas the former are strictly anaerobic and sediments are its main sources to methionine), but also in coenzymes processes, the latter can occur aerobically O ceanography Society. Society. ceanography O the ocean. In addition, the reduced inor- (e.g., coenzyme A, biotin, thiamine) as well as anaerobically, with either oxy- ceanography Society. Send all correspondence to: [email protected] or Th e [email protected] Send Society. ceanography to: all correspondence ganic forms of sulfur, with oxidation in the form of iron-sulfur clusters in gen or nitrate acting as electron accep- tors, or in anoxygenic, anaerobic photo- synthesis. The latter process can play an A ll rights reserved. Permission is granted to copy this article for use in teaching and research. article use for research. and this copy in teaching to granted ll rights reserved. is Permission The global sulfur cycle depends on the important role in microbial mats or eux- activities of metabolically and phylogenetically inic (anoxic and sulfidic) water columns, such as the Black Sea (e.g., Koblizek et al., diverse microorganisms, most of which 2006), but they will not be further dis- reside in the ocean. cussed here. In addition, the metabolism of organic sulfur compounds is a key component of the global sulfur cycle. states of –2 and 0 (as in elemental sulfur) metalloproteins, and in bridging ligands Although the microorganisms car- O are quite common in anoxic environ- (molecules that bind to proteins, for rying out different reactions of the sul- ceanography Society, P Society, ceanography ments, with sulfur compounds of mixed example, in cytochrome c oxidase). valence states (e.g., thiosulfate and poly- Microorganisms can use inorganic sul- STEFAN M. SIEVERT ([email protected]) thionates) produced transiently. The fur, mainly sulfate, to form these organic is Associate Scientist, Biology Department, natural release of volatile organic sulfur compounds in an energy-dependent Woods Hole Oceanographic Institution, O Box 1931, compounds from the ocean, mainly as process referred to as assimilation. Woods Hole, MA, USA. RONALD P. KIENE dimethyl sulfide (DMS), transports sul- However, animals are dependent on is Professor, Department of Marine Sciences, R ockville, M R epublication, systemmatic reproduction, reproduction, systemmatic epublication, fur from the ocean to terrestrial regions, preformed organic sulfur compounds University of South Alabama, Mobile, and it also affects atmospheric chemistry to satisfy their sulfur needs. In addi- AL, USA. HEIDE N. SchULZ-VOGT is D 20849-1931, and the climate system (Figure 1). While tion to assimilation, many bacteria and Juniorprofessor, Institute for Microbiology, they remain very important, natural sul- archaea can use sulfur in energy-yielding Leibniz University, Hannover, Germany. U S A . Oceanography June 2007 117 Volcanic emission (e.g., SO2) UV Radiation (atmospheric photochemistry) Atmospheric deposition Organic Sulfur compounds (e.g., DMS) 1 Photic Zone DMS Deposition Sulfate DMSP Nutrient 3 Hydrothermal vent site Upwelling Emiliania huxleyi MeSH Silicibacter pomeroyi Algae 2 Thiomargarita namibiensis Deposition 2- H2S/NO3 + 2- Hydrogen sulfide NH4 /SO4 S0-globules Sulfate Hydrothermal circulation Figure 1. Diagram illustrating where the cycling of sulfur compounds plays a prominent role in the ocean. (1) In the upper water column, metabolism of organic sulfur com- pounds is of particular relevance. Dimethylsulfoniopropionate (DMSP) pro- duced by algae (e.g., Emiliana huxleyi) is utilized by a diverse assemblage of microbes (e.g., Silicibacter pomeroyi), leading either to the production of methanethiol (MeSH) or dimethylsulfide (DMS), both of which are highly reactive volatile compounds that can escape to the atmosphere. (2) On the continental shelf, sulfate reduction contributes significantly to organic-matter degradation. The hydrogen sulfide produced can be re-oxidized by so-called colorless sulfur-oxidizing bacteria (e.g., Thiomargarita namibiensis). These processes are of particular importance in coastal upwelling regions, such as off the coast ofN amibia, where Thiomargarita namibiensis becomes abundant. It is also in these regions that large sedimentary deposits of phosporites are found. (3) At deep-sea hydrothermal vents, sulfate precipitates out of seawater as anhydrite (CaSO4) at temperatures above 150°C. However, hydrogen sulfide is produced by leaching sulfur from basalt at high temperatures (~ 400°C) in the oceanic crust. The hydrogen sulfide contained in the ensuing reduced hydrothermal fluids is utilized in energy-yielding reactions by free-living and symbiotic sulfur-oxidizing microbes, providing the basis for the lush animal communities found at deep-sea vents. On land, volcanic emissions are the main natural sources of sulfur to the atmosphere. Photochemical processes in the atmosphere oxidize various sulfur species. fur cycle are extremely diverse, most of the sulfur cycle has multiple ties to the HABITATS them belong to the bacterial domain cycles of other elements, most notably Photic Zone (Figure 2). Sulfur-metabolizing archaea those of carbon, nitrogen, phospho- The sulfur cycle of the surface ocean are mainly restricted to high-temperature rous, and iron. Below, we highlight three begins with the assimilatory uptake of environments, such as deep-sea hydro- marine habitats where sulfur cycling is sulfate by phytoplankton (both eukary- thermal vents. Sulfur cycling in the bio- particularly important, namely, the pho- otic algae and prokaryotic cyanobacte- sphere is very rapid, and microorganisms tic zone of the coastal and open ocean, ria) (Figure 1). Some sulfate is incor- in the ocean play an essential role. As a continental margin sediments, and deep- porated, in oxidized form, into sulfated result of the activities of these microbes, sea hydrothermal systems. polysaccharides (e.g., mucus), but most 118 Oceanography Vol. 20, No. 2 Crenarchaeota Euryarchaeota Archaea Thermoproteales Archaeoglobales Desulfurococcales Thermococcales SulfolobalesCrenarchaeota EuryarchaeotaThermoplasmatales Archaea Thermoproteales ArchaeoglobalesSome methanogens, e.g., Methanosarcina Desulfurococcales Thermococcales Sulfolobales Thermoplasmatales Some methanogens, e.g., Methanosarcina Bacteria Nitrospiraceae Bacteria Thermodesulfovibrio A-Proteobacteria Nitrospiraceae Thermodesulfovibrio Roseobacter-cladeA-Proteobacteria, SAR-11 ParacoccusRoseobacter-clade, SAR-11 Various genera,Paracoccus e.g., Rhodobacter, RhodospirillumVarious , genera,Rhodomicrobium e.g., Rhodobacter, Rhodospirillum , Rhodomicrobium Aquificae B-Proteobacteria AquificaeAquifex, Persephonella, B AquifexSulfurihydrogenibium, Persephonella, Thiobacillus-Proteobacteria, Thiomonas Sulfurihydrogenibium Thiobacillus, Thiomonas Desulfurobacterium, Thermovibrio, Alcaligenes Desulfurobacterium, Thermovibrio, Alcaligenes Balnearum Rubrivivax , Rhodocyclus, Rhodoferax Balnearum Rubrivivax , Rhodocyclus, Rhodoferax G ThermodesulfobacteriaceaeThermodesulfobacteriaceae -ProteobacteriaG-Proteobacteria Thermodesulfatator,Thermodesulfatator, Various genera,Various e.g.,genera, Thiomicrospira e.g., Thiomicrospira, Beggiatoa, Beggiatoa, , ThermodesulfobacteriumThermodesulfobacterium ThioplocaThioploca, Thiomargarita, Thiomargarita SymbiontsSymbionts of invertebrates of invertebrates (e.g. , Riftia (e.g. , ,Riftia Calyptogena, Calyptogena) ) Chloroflexaceae Methylophaga, Pseudomonas, Chloroflexaceae Methylophaga, Pseudomonas, ChloroflexusChloroflexus UnidentifiedUnidentified Gammaproteobacteria Gammaproteobacteria ChromatiaceaeChromatiaceae , Ectothiorhodospiraceae , Ectothiorhodospiraceae Firmicutes Desulfotomaculum,Firmicutes Desulfotomaculum, D-Proteobacteria Desulfosporosinus D AmmonifexDesulfosporosinus
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