REVIEWS Microbial ecology of expanding oxygen minimum zones Jody J. Wright1, Kishori M. Konwar1 and Steven J. Hallam1,2 Abstract | Dissolved oxygen concentration is a crucial organizing principle in marine ecosystems. As oxygen levels decline, energy is increasingly diverted away from higher trophic levels into microbial metabolism, leading to loss of fixed nitrogen and to production of greenhouse gases, including nitrous oxide and methane. In this Review, we describe current efforts to explore the fundamental factors that control the ecological and microbial biodiversity in oxygen-starved regions of the ocean, termed oxygen minimum zones. We also discuss how recent advances in microbial ecology have provided information about the potential interactions in distributed co‑occurrence and metabolic networks in oxygen minimum zones, and we provide new insights into coupled biogeochemical processes in the ocean. Ventilated Over geological time the ocean has evolved from being ecosystems and pelagic ecosystems reduces, changing Pertaining to the ocean: an anaerobic incubator of early cellular existence into the species composition and food web structure in supplied with atmospheric 15 a solar-powered emitter of molecular oxygen (O2), a these regions . Organisms that are unable to escape gases through processes transformation that has been punctuated by catastrophic O -deficient conditions may experience direct mortal- including exchange between 2 the air and sea, exchange extinctions followed by the iterative re-emergence of bio- ity (that is, the fish in these regions die) or decreased fit- 1,2 16,17 between the surface mixed logical diversity . Today, the ocean is being transformed ness . Even organisms that can escape to more highly layer and immediate in response to human activities. Indeed, the fourth assess- oxygenated refuges are susceptible to increased preda- subsurface layer, and ment report of the Intergovernmental Panel on Climate tion and density-dependent reductions in population circulation in the interior Change observed that the ocean is becoming substan- size18. OMZ expansion also causes changes in the cycling of the ocean. 3 tially warmer and more acidic . As these changes inten- of trace gases such as methane (CH4), nitrous oxide sify, marine ecosystems will experience disturbances in (N2O) and carbon dioxide (CO2), which are important the structure and dynamics of food webs, with resulting for metabolism and can have an effect on climate. CH4 4 radiative feedback on the climate system . Oxygen-starved regions and N2O are powerful greenhouse gases with of the ocean, known as oxygen minimum zones (OMZs), forcing effects that are approximately 25 and 300 times 5 are important bellwethers for these changes . the effect of CO2, respectively. Although oceanic CH4 OMZs are an intrinsic feature of water columns emissions are minor (<2% of natural CH4 emissions), the 1 Department of Microbiology that arise when the respiratory O2 demand during the ocean accounts for at least one-third of all natural N2O and Immunology, University degradation of organic matter exceeds O2 availability emissions, a large fraction of which are derived from of British Columbia, ventilated 6–9 − in poorly regions of the ocean . Increases OMZs via microbial respiration of nitrate (NO3 ) and Life Sciences Institute, − 19 2552–2350 Health Sciences in ocean temperature drive decreases in O2 solubility nitrite (NO2 ) . Moreover, OMZs account for up to 50% Mall, Vancouver, British and reduced ventilation owing to thermal stratification of oceanic fixed-nitrogen loss, and their expansion has Columbia V6T 1Z3, Canada. of the water column8,10, resulting in OMZ expansion. the potential to affect primary production, with resulting 2Graduate Program in Consistent with this, between 1956 and 2006 the O con- feedback on carbon transport processes20–23. Bioinformatics, University of 2 British Columbia, Life Sciences centrations in the OMZ of the northeast subarctic Pacific Although OMZs are inhospitable to aerobically Institute, 2552–2350 Health (NESAP) declined by 22%, and the hypoxic boundary respiring organisms, these zones support thriving micro- Sciences Mall, Vancouver, layer (defined as ~60 μmol O2 per kg water) expanded bial communities that mediate cycling of nutrients and British Columbia V6T 1Z3, upwards from a depth of 400 m to 300 m (REF. 11). Similar radiatively active trace gases (which affect the climate). Canada. declines have been observed in the eastern tropical Therefore, systems-level investigations of microbial Correspondence to S.J.H. 12 12 13,14 e‑mail: Atlantic , the equatorial and northeast Pacific, and communities in the OMZ-containing water column 8 [email protected] in the Southern Ocean during the past 50 years. have great potential to enhance our mechanistic under- doi:10.1038/nrmicro2778 As O2 concentrations decline, the amount of habitat standing of a pervasive ecological phenomenon that Published online 14 May 2012 available to aerobically respiring organisms in benthic is integral to ocean productivity and climate balance. NATURE REVIEWS | MICROBIOLOGY VOLUME 10 | JUNE 2012 | 381 © 2012 Macmillan Publishers Limited. All rights reserved REVIEWS Here, we review recent observations that have emerged western Pacific (where Pacific deep waters are formed) from the intersection of taxonomic and functional gene as well as to the length of time that these waters have surveys, gene expression studies and measurements of been isolated from the atmosphere (a result of global process rates to better formulate hypotheses regarding circulation patterns). However, O2 deficiency is often the metabolic interactions that drive OMZ ecology and more intense in the Arabian Sea and in coastal Atlantic biogeochemistry on a global scale. We focus on bacte- waters on the African shelf than in the Pacific Ocean rial and archaeal contributions to these networks, with owing to unusually high levels of carbon export and sub- the understanding that microbial eukaryotes and viruses surface respiration in these naturally eutrophic waters of have biologically essential but as-yet physiologically the Arabian Sea and Atlantic Ocean29. Compounding the uncharacterized roles in modulating matter and energy effects of respiratory demands for O2, many upwelling transformations in OMZs. systems experience episodic plumes of hydrogen sul- phide (H2S) that can be attributed to diffusive flux from OMZ formation and expansion underlying sediments30. Such sulphidic events are toxic OMZs are typically found on the western boundaries to most O2-respiring organisms. In addition to coastal of continental margins, where wind-driven circulation and open-ocean OMZs, enclosed or semi-enclosed patterns push nutrient-rich waters upwards to the sur- basins — including the Baltic Sea31, Black Sea32, Cariaco face in a process known as coastal upwelling. This process Basin33 and Saanich Inlet34 — experience varying degrees Thermal stratification effectively fertilizes surface waters and results in high of O2 deficiency and sulphide accumulation, making A temperature-layering effect levels of photosynthetic primary production. During them useful model ecosystems for exploring microbial that occurs in water owing to photosynthesis, phytoplankton fix CO2. Much of the community responses to OMZ expansion. differences in water density: inorganic carbon that is fixed through photosynthesis is Human activities exacerbate the natural O2 defi- warm water is less dense than respired in surface and intermediate layers of the water ciency in shallow coastal and estuarine environments, cool water and therefore tends to float on top of the cooler, column through microbial degradation processes. A where nutrient run-off from agricultural and wastewater 35 heavier water. fraction of the product of primary production sinks as sources results in eutrophication . Moreover, changes in dead organisms and particles that are exported to depth. wind-driven circulation patterns can induce upwelling Benthic ecosystems Throughout the ocean this process, called the biological of O -deficient waters from coastal OMZs onto conti- Ecosystems residing at the 2 lowest level of a body of water carbon pump, has a large influence on the biogeochemi- nental shelves, increasing mortality of shelf-dwelling 36 such as an ocean or a lake, cal carbon cycle because carbon is sequestered in the organisms . Over the past two decades, shelf intrusions including the sediment surface interior of the ocean for long periods of time, during have produced ‘dead-zones’ off coastal Oregon37 and in and subsurface layers. which it cannot influence the climate24. Estimates of the Gulf of Mexico38 (USA), and off the coast of Chile28, carbon rain rates to carbon sediments in the northeast Africa39 and India40, contributing to a drop in produc- Pelagic ecosystems 35 Ecosystems residing in the Pacific suggest that the presence of an OMZ greatly tion from commercial fisheries . Regardless of the water region of a body of water that increases the amount of carbon exported to the deep body (estuary, basin, coastal waters or open ocean), O2 is neither close to the bottom ocean25. deficiency shifts energy away from a pelagic macrofauna nor near the shore. Persistent O2 deficiency occurs when the amount of towards microorganisms, decoupling predator–prey Radiative forcing effects dissolved O2 in the water column is consumed faster than interactions and changing the trophic exchanges that The change in net irradiance it is resupplied through