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> Section IV. Processes

Oceanography > Chapter 9. Microbes and Major Elemental Cycles , V olume 20, N olume The Cycle By Stefan M. Sievert, Ronald P. Kiene, and Heide N. Schulz-Vogt umber 2, a quarterlyumber The O journal of

The ocean represents a major fur emissions have currently been over- reactions, called dissimilatory sulfur of sulfur on Earth, with large quanti- taken by anthropogenic emissions, pri- . These latter processes are ties in the form of dissolved and marily from the burning of fossil fuels. essential for the cycling of sulfur on our

ceanography Society. Copyright 2007 by The O sedimentary minerals (e.g., Sulfur is an essential element for . planet, and will be the primary subject and ). 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 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 (primarily the tion and sulfur oxidation, respectively. Earth; and leaching of rocks S-containing amino acids, and Whereas the former are strictly anaerobic and sediments are its main sources to ), but also in coenzymes processes, the latter can occur aerobically ceanography Society. A 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:ceanography Society. Send [email protected] Th e O or 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 ll rights reserved. Permission is reserved. ll rights granted to in teaching copy this and research. for use article R the global 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- are quite common in anoxic environ- (molecules that bind to , for rying out different reactions of the sul- ceanography Society, P ments, with sulfur compounds of mixed example, in cytochrome c oxidase). valence states (e.g., 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, Department, natural release of volatile organic sulfur compounds in an energy-dependent Woods Hole Oceanographic Institution, Box 1931, R O Box compounds from the ocean, mainly as process referred to as assimilation. Woods Hole, MA, USA. Ronald P. Kiene (DMS), transports sul- However, are dependent on is Professor, Department of Marine Sciences, ockville, M D 20849-1931, U ockville, epublication, systemmatic , 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 and the climate system (Figure 1). While tion to assimilation, many and Juniorprofessor, Institute for , they remain very important, natural sul- can use sulfur in energy-yielding Leibniz University, Hannover, Germany. S A .

Oceanography June 2007 117 Volcanic emission (e.g., SO2)

UV Radiation (atmospheric photochemistry) Atmospheric deposition Organic Sulfur compounds (e.g., DMS) 1 DMS Deposition Sulfate DMSP

Nutrient 3 site Upwelling Emiliania huxleyi MeSH Silicibacter pomeroyi

Algae 2 Thiomargarita namibiensis Deposition 2- H2S/NO3

+ 2- 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 . (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 as (CaSO4) at temperatures above 150°C. However, hydrogen sulfide is produced by leaching sulfur from basalt at high temperatures (~ 400°C) in the oceanic . 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 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 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 (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. (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 -ProteobacteriaVarious genera, e.g., Desulfovibrio, Desulfotalea Ammonifex Various genera,Desulfonema e.g., ,Desulfovibrio Desulfosarcina, , DesulfotaleaDesulfobacter DesulfonemaDesulfuromonas, Desulfosarcina, Desulfurella, Desulfobacter, Desulfuromusa, Chlorobiaceae DesulfuromonasGeobacter, Desulfurella, Desulfuromusa, E-Proteobacteria Chlorobiaceae GeobacterSome sulfate reducers, e.g., Desulfovibrio E-ProteobacteriaArcobacter, Thiovulum, Sulfurimonas, Some sulfate reducers, e.g., Desulfovibrio ArcobacterSulfurovum, Thiovulum, Sulfurimonas, SulfurovumVarious genera, e.g., Sulfurospirillum, VariousNautilia genera,, Caminibacter e.g., Sulfurospirillum, Nautilia, Caminibacter

Phototrophic sulfur-oxidizers Chemolithotrophic sulfur-oxidizers Sulfur reducers Sulfate reducers Organic sulfur utilizers

PhototrophicFigure 2. Schematic sulfur-oxidizers phylogenetic treeChemolithotrophic depicting the distribution sulfur-oxidizers of different types of sulfur-metabolizingSulfur reducers microorganismsSulfate among reducers major phylogeneticOrganic lineages. sulfur Allutilizers forms of can be found within the proteobacteria, whereas as other lineages are more restricted in their physiological repertoire. Note that the capability to convert DMSP into DMS is widespread among bacteria, and that not all of the lineages with members capable of this conversion are shown in the tree. Adapted from Giovannoni and Stingl (2005)

is assimilated into methionine and cys- grazing deterrent (Stefels, 2000; Sunda accounts for about 50 x 1012 moles of teine. Methionine is converted by some et al., 2002). Diatoms produce rela- sulfur per year. Because each molecule phytoplankton into dimethylsulfonio- tively low amounts of DMSP (1–50 mM of DMSP contains five atoms of carbon, propionate (DMSP) (Gage et al., 1997), intracellular concentrations), but DMSP synthesis is also important in the a highly stable and soluble form of dinoflagellates, prymnesiophytes, and ; its production is estimated reduced sulfur. Because of its high cyto- some chrysophytes produce very large to account for 3–10% of the global plasmic concentrations, DMSP func- amounts (100–300 mM intracellular marine primary production of carbon tions as an osmolyte, but it also has other concentrations). On the whole, DMSP (Kiene et al., 2000), and its degradation functions, such as an antioxidant and synthesis by marine photoautotrophs supplies about 3–10% of the carbon

Oceanography June 2007 119 requirements of heterotrophic bacteria by microorganisms. The assimilation Marine Sediments in surface waters (Simó et al., 2002). of MeSH occurs by an elegant reaction As soon as organic material settles on

The importance of DMSP in biogeo- whereby the entire CH3S group is incor- the seafloor, oxygen is rapidly exhausted is magnified by its role porated directly into methionine (Kiene and sulfate is used as an electron accep- as the main precursor of volatile DMS. et al., 2000). A large fraction of the active tor by sulfate-reducing DMS emissions from the surface ocean bacteria in surface seawater assimilates (SRP) to oxidize organic material to the atmosphere range from 0.5 to sulfur from DMSP, with members of (Figure 1). As a result of this anaerobic 1.0 x 1012 moles per year (Kettle and the α- and γ-proteobacteria being par- respiration, which accounts for up to Andreae, 2000). In the atmosphere, DMS ticularly important (Malmstrom et al., 50% of organic carbon mineralization is oxidized to acidic aerosol particles that 2004). Even photoautotrophs such as in ocean margin sediments (Jørgensen, affect cloud properties and the amount and diatoms assimilate 1982), large amounts of foul-smelling of solar radiation reflected back to space sulfur from dissolved DMSP (Vila- sulfide are produced. Some of the (Charlson et al., 1987). Thus, DMS pro- Costa et al., 2006a), although it remains energy in the original organic matter is duction by the plankton community unclear whether they assimilate DMSP conserved in the sulfide, and it can be can influence climate, and the potential directly or whether they obtain the sulfur released by a special group of bacteria, exists for DMS-linked climate feedbacks from MeSH produced by other organ- the large, vacuolated sulfur bacteria of to the plankton (Charlson et al., 1987). isms. Interestingly, DMSP contributes the genera Beggiatoa, Thioploca, and Some phytoplankton that produce 50–100% of the sulfur required for het- Thiomargarita. They occur as dense DMSP have enzymes that cleave DMSP erotrophic bacterial biomass production mats in sediments of coastal upwell- into DMS and acrylic acid. Bacteria from (Kiene et al., 2000). This is remarkable ing areas (e.g., Chile, Peru, Namibia, diverse lineages also can convert dis- considering seawater contains 1–10 mil- Arabian Sea), at whale carcasses, at solved DMSP into DMS (Yoch, 2002), lion times more sulfate than DMSP. hydrothermal vents and seeps, at meth- but the amount of DMS produced by In addition to funneling most of the ane hydrates, but also in quite ordi- bacteria is limited by the fact that they DMSP away from DMS production, nary eutrophic coastal environments metabolize most (e.g., 80–90%) of the bacteria control the emissions of DMS such as fjords or salt marshes (Teske DMSP by a demethylation pathway that by consuming a large fraction of the and Nelson, 2006). does not produce DMS (Kiene et al., DMS produced and converting it into These three closely related genera are 2000). Instead, this alternative pathway the nonvolatile products dimethyl sulf- adapted to oxidize sulfide, even when results in formation of methiolpro- oxide (DMSO) and sulfate (del Valle et oxygen is absent, by using nitrate as the pionate and, subsequently, methane- al., 2007). We are only beginning to learn electron acceptor. To be able to com- thiol (CH3SH; MeSH). The gene that which organisms might be involved in pete with other sulfide oxidizers, they encodes for the key DMSP demethylat- DMS consumption. A recent experimen- monopolize this metabolism, storing ing enzyme, dmdA, was only recently tal study shows that Methylophaga spp., nitrate from the bottom water inter- discovered in the genomes of Silicibacter a genus known to metabolize DMS, is a nally in a vacuole and transporting the pomeroyi and Candidatus Pelagibacter prominent group that developed in sea- nitrate into the sediment, where sulfide ubique, and it appears to be prevalent water enriched with DMS (Vila-Costa is produced (Fossing et al., 1995). To in members of the numerically impor- et al., 2006b). Ultimately, only 1–2% of store as much nitrate as possible, they tant Roseobacter and SAR11 clades the synthesized DMSP sulfur is released have to enlarge their vacuoles, and, as (Howard et al., 2006). to the atmosphere as DMS, yet this small a result, this group of bacteria con- Because MeSH is so reactive, very little leak from the DMSP/DMS biogeochemi- tains many giant forms easily visible to escapes to the atmosphere. Most of the cal system is responsible for the massive the naked eye, with cell diameters of MeSH produced is oxidized, and some transfer of sulfur from the oceans to the 0.1–0.75 mm (Schulz et al., 1999). The is assimilated into sulfur amino acids atmosphere and ultimately to land. large sulfur bacteria respire nitrate, but

120 Oceanography Vol. 20, No. 2 in contrast to denitrifying bacteria, they Deep-Sea Hydrothermal Vents Besides the well-known γ-proteobacte- seem to reduce the nitrate to ammo- Deep-sea hydrothermal vents are highly rial sulfur-oxidizers like Beggiatoa spp., nia and not to N2. This has important productive , where chemo- Thiomicrospira spp., and endosymbionts consequences for the nitrogen budget lithoautotrophic microorganisms medi- of invertebrates (e.g., Riftia pachyptila), of their habitats, as ammonia can be ate the transfer of energy from the bacteria belonging to ε-proteobacte- re-oxidized to nitrate and stay within geothermal source to the higher tro- ria have only recently been recognized the system. Additionally, these bacteria phic levels (Jannasch and Mottl, 1985). as important members of the micro- store polyphosphate, which they release Dissimilatory sulfur metabolism is a bial communities at deep-sea vents periodically as phosphate, leading to key component driving these systems, (Campbell et al., 2006). Novel sulfur- rapid precipitation of phosphorous- with sulfur oxidation being of particu- oxidizing ε-proteobacteria belonging to containing minerals. Thus, they can also lar importance. At deep-sea vents, H2S the genus Arcobacter produce sulfur in play an important role in phosphorous is produced geothermally within the filamentous form that is morphologi- cycling in the sediment by removing oceanic crust as a result of rock-seawa- cally and chemically similar to material phosphorous from the (Schulz ter interactions at high temperatures observed after deep-sea volcanic erup- and Schulz, 2005). The metabolism rather than as a result of dissimilatory tions (Taylor and Wirsen, 1997; Sievert of organic sulfur compounds is also sulfate reduction (Figure 1). The ensu- et al., 2007). These microbes might also important in sedimentary habitats. For ing hot hydrothermal fluids contain high be part of a subseafloor biosphere, which example, DMS is used by aerobes like concentrations of H2S (usually around is, at present, a poorly defined, yet criti- Methylophaga spp. and Hyphomicrobium 3–10 mM), but no sulfate, which pre- cally important component of deep-sea spp. as well as strict anaerobes such cipitates as anhydrite at temperatures hydrothermal systems (Wilcock et al., as the methylotrophic methanogens > 150˚C. Currently, not much is known 2004). Interestingly, these and many in the domain Archaea. DMS can also about the metabolism of organic sulfur other autotrophic microorganisms pres- be formed in anoxic habitats from the compounds at deep-sea vents, although ent at deep-sea vents use the reductive methylation of sulfide and methanethiol, this might potentially be an important tricarboxylic acid cycle for autotrophic a process that may support some of the process (e.g., Schulte and Rogers, 2004). , questioning the para- anaerobic methylotrophs. In areas where small amounts of organic material settle on the seafloor, in the future, it will be important to sulfate is only used up slowly and may still be present several hundred meters improve quantitative estimates of these down into the sediment (D’Hondt et processes and to learn more about al., 2004). At some sites on the Peruvian shelf, sulfate is depleted in surface sedi- their interdependencies. ments but becomes available again at greater depths from an underlying ancient brine. Thus, sulfate can be an The large supply of H2S fuels sul- digm that the well-known Calvin cycle important electron acceptor for bacteria fur-oxidizing bacteria that exist either is at the base of deep-sea hydrother- populating the deep biosphere. Here, as free-living forms in the mixing zone mal ecosystems (Campbell et al., 2006 as well as in other anaerobic environ- between oxygenated seawater and the and references therein; Hügler et al., ments, it may be used as an electron highly reduced hydrothermal fluids, 2007; Markert et al., 2007). Recently, acceptor by a microbial consortium above or below the seafloor, or in a sym- the genomes of a number of either free- oxidizing the greenhouse gas methane biotic relationship with various inver- living or symbiotic sulfur-oxidizing (Widdel et al., 2004). tebrates (Jannasch and Mottl, 1985). bacteria have become available, greatly

Oceanography June 2007 121 facilitating progress in our understand- ter serve as carbon sources for sulfate- interdependencies. Such knowledge will ing of this important process and the reducing prokaryotes at this vent site enable us to better assess their envi- development of functional gene assays to (Widdel et al., 2004). Studies based on ronmental impact and their possible assess the diversity and activity of these the detection of a gene coding for a key responses to environmental changes. At organisms in situ (Scott et al., 2006; enzyme of sulfate reduction (i.e., dissim- present, we have only limited ability to Markert et al., 2007; Newton et al., 2007; ilatory ) further reveal identify the actual microbial “players” Sievert et al., in press). Interestingly, that many SRP exist in these environ- and to couple the identity of the organ- the presence of a gene cluster predicted ments that are currently not represented isms with their functions and activities to encode proteins involved in pho- in culture collections (e.g., Dhillon et al., in situ. New developments in sensor sponate utilization in the genome of 2003), indicating that we might yet have technology to measure rates in situ and the free-living, sulfur-oxidizing bacte- to characterize the real “players.” the availability of genomes, in combina- rium Thiomicrospira crunogena XCL-2 tion with metagenomic and microbio- suggests that phosphate could poten- Conclusions and Future logical approaches, will facilitate prog- tially be a limiting nutrient at deep-sea Prospects ress along these lines. hydrothermal vents, similar to what has The global sulfur cycle depends on the been described for the marine cyano- activities of metabolically and phyloge- Acknowledgements bacterium Trichodesmium erythraeum, netically diverse microorganisms, most Preparation of this manuscript was par- which thrives in phosphate-depleted of which reside in the ocean. Although tially supported by National Science surface waters (Dyhrman et al., 2006; sulfur rarely becomes a limiting nutri- Foundation grant OCE-0452333 Scott et al., 2006). ent, its turnover is critical for and a fellowship from the Hanse- Elemental sulfur (S0) is a key substrate function. Organic sulfur compounds fuel Wissenschaftskolleg (http://www. at hydrothermal vents, particularly at in the upper water h-w-k.de) to SMS, National Science higher temperatures, as a number of column and their turnover has impor- Foundation grants OPP-0230497 thermophilic and hyperthermophilic tant consequences, for example, for the and OPP-0083078 to RPK, as well as bacteria and archaea can use S0 as an climate system. Changes in phyto- and the Research Center Ocean Margins electron donor in either autotrophic or bacterioplankton composition due to (RCOM) of the University of Bremen heterotrophic metabolism (e.g., Stetter, global change could thus have dramatic, (Germany) to HNSV (RCOM-Nr. 0476). 2006). Some of these organisms can also but as yet poorly understood, ramifica- We thank Paul Oberlander (WHOI use nitrate as an alternative electron tions. Sulfur-metabolizing microorgan- Graphic Services) for preparing the fig- acceptor (e.g., Vetriani et al., 2004). In isms also fulfill essential functions in ures, as well as Ellen Kappel and Vicky addition, many hyperthermophiles use their habitats by either degrading or Cullen for editorial help. We extend S0 as an electron sink during fermenta- forming biomass (organic carbon), as our gratitude to Dave Karl and Lita tion. At Guaymas Basin, a sediment- exemplified by the degrading activities Proctor for initiating and organizing covered deep-sea vent site, microbial of sulfate-reducing bacteria in marine this special issue. sulfate reduction occurs at temperatures sediments and the formation activities up to 110°C, which exceeds the maxi- of sulfur-oxidizing bacteria at deep- References mum growth temperature for cultivated sea hydrothermal vents. Some sulfur- Campbell B.J., A.S. Engel, M.L. Porter, and K. Takai. 2006. The versatile ε-proteobacteria: Key hyperthermophilic sulfate reducers of oxidizing bacteria further increase players in sulphidic habitats. Nature Reviews the genus Archaeoglobus (Jørgensen et ecosystem productivity by retaining Microbiology 4:458–468. Charlson, R.J., J.E. Lovelock, M.O. Andreae, and al., 1992). In addition, liquid and gas- nitrogen and phosphorous compounds. S.G. Warren. 1987. Oceanic phytoplankton, eous aliphatic and aromatic hydrocar- In the future, it will be important to atmospheric sulfur, cloud albedo and climate. Nature 326:655–661. bons generated by hydrothermal heating improve quantitative estimates of these D’Hondt S., B.B. Jørgensen, D.J. Miller, A. Batzke, of immature sedimentary organic mat- processes and to learn more about their R. Blake, B.A. Cragg, H. Cypionka, G.R.

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