486 Chem. Rev. 2007, 107, 486−513 Oceanic Methane Biogeochemistry William S. Reeburgh* Department of Earth System Science, University of California, Irvine, California 92697-3100 Received June 23, 2006 Contents 10. Summary 507 11. Future Work 507 1. Introduction 486 11.1. Natural 14C Measurements on Ocean Water 507 1.1. Global Methane Budget 487 Column Methane 1.2. Role of the Ocean in the Global Methane 487 11.2. Oxidation Rate Measurements 507 Budget 11.3. Mixed Layer Maximum 508 2. Ocean Methane Measurements 488 11.4. Methane-Consuming Benthic Communities 508 2.1. Water Column 488 11.5. Hydrate Dissociation 508 2.2. Sediments 488 11.6. Molecular Genetics, Reaction Mechanism, 508 2.3. Headspace Measurements 489 and Biomarkers 2.4. Natural Isotopes 489 11.7. Sensors 509 3. Oceanic Water Column Methane Distributions 489 11.8. Mud Volcanoes 509 4. Methane Distributions in Sediments 490 12. Acknowledgments 509 5. Water Column Methane Production? 492 13. Note Added in Proof 509 5.1. Thermodynamic, Kinetic, and Physical 492 14. References 509 Constraints on Water Column Methane Production 5.2. Methanogenesis Involving Noncompetitive 493 1. Introduction Substrates Measurements of dissolved methane in the ocean have 5.3. Microenvironments and the Ocean Methane 493 been available for only about 50 years. Methane measure- Paradox ments in sediments, where concentrations are millimolar, 6. External Water Column Methane Sources 494 were first reported in the mid-1950s, while measurements 6.1. Production Processes 494 of methane in ocean waters, where concentrations are 6.1.1. Diagenesis of Organic Carbon 494 nanomolar, were first reported in the late 1960s. 6.1.2. Hydrothermal Systems and the 494 Methane is the most abundant hydrocarbon in the atmo- Serpentinization Reaction sphere, where it plays an important role in tropospheric 6.1.3. Methane Clathrate Hydrate 495 atmospheric chemistry. Further, methane is an important Decomposition greenhouse gas. Atmospheric time series observations over 6.2. Transport Processes: Scope and Scale 496 the past two decades have documented an increase in the 6.2.1. Coastal Contributions 496 atmospheric mixing ratio of methane, and a great deal of 6.2.2. Seeps and Vents 497 activity has focused on the cause and climate consequences 6.2.3. Mud Volcanoes 497 of this increase. The ocean contributes a relatively small 7. Microbially-Mediated Oxidation of Ocean Methane 498 amount of methane to the global net atmospheric budget, 7.1. Aerobic Oxidation of Methane 498 and it cannot be expected to play a role in the contemporary atmospheric methane increase. Our interest in methane in 7.2. Anaerobic Oxidation of Methane 498 the ocean is understanding the balance between the enormous 7.2.1. Early Observations and the Methane/ 498 reported methane additions from continental shelf and slope Sulfate Connection sediments and the microbial oxidation reactions that must 7.2.2. Rate Measurements 500 occur in sediments and the water column to produce the low 7.2.3. Natural Isotope Studies 501 nanomolar concentrations observed in the bulk of the ocean 7.2.4. Reaction and Mechanism 503 volume. 7.2.5. Isotopically Light Carbonates 503 A number of poorly quantified external sources contribute 8. New Tools and Recent Developments 504 methane to the ocean water column. The source processes 8.1. Biomarkers 504 include microbially-mediated diagenesis of sediment organic 8.2. Physiological and Culture-Independent 504 matter, abiotic production of methane through the serpenti- Phylogenetic Studies nization reaction, a rock/water reaction occurring in hydro- 8.3. Methane-Utilizing Communities 505 thermal systems associated with the midocean ridges and 9. Summary of Ocean Methane Sources and Sinks 505 spreading centers, leaks from near-surface petroleum depos- its, and decomposition of methane clathrate hydrates. These * E-mail: [email protected]. Telephone: 949-824-2986. Fax: 949-824- contributions enter the ocean water column through coastal 3874. runoff, by diffusion from organic-rich anoxic sediments, and 10.1021/cr050362v CCC: $65.00 © 2007 American Chemical Society Published on Web 01/30/2007 Oceanic Methane Biogeochemistry Chemical Reviews, 2007, Vol. 107, No. 2 487 effective methane consumer or sink fueled by external sources. Since oxidation is so nearly quantitative, aerobic and especially anaerobic methane oxidation rates are sum- marized and integrated to estimate methane fluxes from the external sources outlined above. This paper also covers recent developments in biomarker molecules, genomics, and benthic communities apparently sustained by methanotrophy, and it outlines fruitful areas for future research. Recent reviews on global methane biogeochemistry1-4 emphasize contributions from a number of sources, the use of natural stable and radioisotopes in quantifying and constraining the sources, and processes contributing to the atmospheric methane increase. Reviews of methane geochem- istry have emphasized several areas: aquatic environments,5,6 anaerobic oxidation of methane,7,8 and recent advances in Bill Reeburgh was born and raised in Port Arthur, Texas. He earned a anaerobic oxidation of methane,9,10 as well as microbiological B.S. in Chemistry at the University of Oklahoma in 1961, and M.A. and aspects of methanogenesis (methane production)11 and Ph.D. degrees in Oceanography at The Johns Hopkins University in 1964 12-14 and 1967. He was on the faculty of the Institute of Marine Science at the methanotrophy (methane consumption) and the role University of Alaska, Fairbanks from 1968 until 1993, when he joined the microbial methane consumption plays in controlling methane University of California Irvine as one of the founding faculty of the Program fluxes to the atmosphere. Methane biogeochemistry is in Geosciences, now the Department of Earth System Science. He was covered in microbial ecology texts,15 but it has received editor of Global Biogeochemical Cycles from 1998 to 2004 and was elected limited attention in chemical oceanography and marine AGU Fellow in 2001. His research focus has been on methane geochemistry texts16-20 and reviews.21 geochemistry, particularly documenting the occurrence and extent of anaerobic oxidation of methane, and recent measurements of natural stable 2 13 14 isotopes ( H-CH4, C-CH4) and radiocarbon ( C-CH4) in methane from 1.1. Global Methane Budget anoxic marine sediments and waters. Any discussion of oceanic methane biogeochemistry through seeps, vents, and mud volcanoes emitting methane- should place the ocean in the context of the global methane rich fluids or methane-rich bubbles. Despite these large and budget. A geochemical budget is a flux balance (or a mass poorly quantified methane additions to the ocean water balance) that provides a useful means of partitioning and column, microbially-mediated aerobic and anaerobic oxida- estimating the magnitudes of sources and sinks. Budgets are tion reactions effectively consume the added methane to low very useful in exposing our ignorance, but they have no nanomolar levels, so that most of the ocean volume is predictive power. undersaturated with respect to the atmosphere. The first global methane budget, a net atmospheric budget, was based on available flux measurements and estimates Methane is produced within ocean waters at only one 22,23 14 location: the nearly ubiquitous surface mixed layer methane from a variety of sources. The natural radiocarbon ( C) maximum, where methane concentrations are ∼5 nM, content of atmospheric methane was used to partition the supersaturated with respect to the atmosphere. Methanogen- budget between recent biogenic and fossil sources. Oxidation esis is mediated by strict anaerobes, and since the vast by OH in the troposphere and destruction in the stratosphere were considered sinks. majority of the ocean water column contains oxygen, the 24-27 presence of this methane maximum presents “the ocean Time series observations beginning in the late 1970s methane paradox”. Anoxic environments in digestive tracts showed that the atmospheric methane mixing ratio was increasing by ∼1% year-1, and methane measurements in and leakage from freshly released fecal pellets have been 28-31 suggested as the major contributor to this enigmatic methane polar ice cores showed that the atmospheric increase maximum. There is no evidence, even in anoxic basins, of started long before it was documented by the atmospheric large-scale methanogenesis at other locations in the water time series observations. The atmospheric mixing ratio increase and recent field measurements were reviewed by column. Curiously, the enigmatic surface mixed layer 1 methane maximum, which also receives contributions from Cicerone and Oremland, who concluded that the atmospheric coastal runoff, amounts to about 25% of the ocean source increase was genuine and proposed a revised methane budget term to the atmosphere in the global methane budget because based on new information on sources and sinks. On the basis of its proximity to the atmosphere. of a framework of constraints involving the global methane Instead of thinking of an ocean methane cycle, where burden, turnover rates, and isotopes, we have high confidence methane participates in a geochemical cycle involving linked in the total budget, the rate of change, the fraction of modern production, utilization, and regeneration reactions, it is more biogenic methane, and the total source (or sink). How to correct to think of the ocean as a large reactor that very apportion the individual sources is less certain. By constrain- effectively oxidizes methane from a wide range of sediment ing the magnitude of the total, this budget served to limit sources. With the exception of the mixed layer methane proliferation of source estimates. Seasonal time series maximum, the ocean methane is produced in sediments and observations at fixed stations were used as a constraint in an inverse model, and several likely global methane budget has a benthic source. Methane is oxidized under anoxic 32 conditions in marine sediments and waters; it is oxidized scenarios were proposed by Fung et al. under oxic conditions at the benthic boundary layer and in the water column.