Microbiology of oxygen minimum zones

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An oxygen minimum zone (OMZ) is characterized as an oxygen-deficient layer in the world's oceans. Typically found between 200m to 1500m deep below regions of high productivity, such as the western coasts of continents. [1] OMZs can be seasonal following the spring-summer upwelling season. Upwelling of nutrient-rich water leads to high productivity and labile organic matter, that is respired by heterotrophs as it sinks down the water column. High respiration rates deplete the oxygen in the water column to concentrations of 2 mg/L or less forming the OMZ. [2] OMZs are expanding, with increasing ocean deoxygenation. Under these oxygen-starved conditions, energy is diverted from higher trophic levels to microbial communities that have evolved to use other biogeochemical species instead of oxygen, these species include Nitrate, Nitrite, Sulphate etc. [3] Several Bacteria and Archea have adapted to live in these environments by using these alternate chemical species and thrive. The most abundant phyla in OMZs are Pseudomonadota, Bacteroidota, Actinomycetota, and Planctomycetota. [3]

Contents

In the absence of oxygen, microbes use other chemical species to carry out respiration, in the order of the electrochemical series. [4] With nitrate and nitrite reduction yielding as much energy as oxygen respiration, followed by manganese and iodate respiration and yielding the least amount of energy at the bottom of the series are the iron and sulfate reducers. the utilization of these chemical species by microbes plays an important role in their biogeochemical cycling in the world's oceans. [5]

Life in anoxic conditions

The nutrient cycles in and around the oxygen minimum zone OMZ cycles.jpg
The nutrient cycles in and around the oxygen minimum zone

Nitrogen Cycling

Biological productivity (photosynthesis) in marine ecosystems is often limited by the bioavailability of nitrogen. [6] The amount of bioavailable nitrogen (nitrate (NO3−), nitrite (NO2−), and ammonium (NH4+)) depends on the inputs from nitrogen fixation and losses from denitrification and anammox as dinitrogen gas (N2), a compound only accessible to nitrogen-fixing bacteria. [7] [6] N2 production from denitrification and anammox closes the nitrogen cycle by reducing the nitrogen available in organic matter fixed by phytoplankton at the surface ocean. Denitrification in OMZs leads to a significant loss of inorganic nitrogen from the oceans, limiting growth/productivity in many regions around the world. OMZs are known for their role in the global nitrogen cycle. As no oxygen is present to fuel aerobic respiration, anoxic systems are primarily dominated by microbially-mediated nitrogen cycling.

N2 fixation is performed by diazotrophs (N2 fixing bacteria and archaea), which convert N2 gas into ammonia (NH3). The amount of N2 fixation and the distribution of diazotrophs in the ocean is determined by the availability of oxygen (O2), light, phosphorus (P), iron (Fe), and organic matter, as well as habitat temperature. N2 fixation has been found in some anoxic systems, generally associated with sulfate reducers or oxidizers. [8] However, heterotrophic denitrification is a more dominant process under anoxic conditions. Denitrification is the reduction of NO3− and NO2− to the gaseous form of nitrogen (N2), including the greenhouse gas nitrous oxide (N2O). [9] Heterotrophic denitrification is a multi-step process that uses organic matter to reduce NO3− to N2 in oxygen-depleted environments like OMZs and sediments. [6] In OMZs, different steps in the denitrification processes are performed by separate groups of bacteria, and these denitrifiers are often found directly on sinking organic matter particles, which are hotspots of microbial activity. [10] [11] The first step of denitrification is nitrate reduction where NO3− is reduced to NO2− by the protein nitrate reductase. Anaerobic ammonia-oxidizing bacteria (anammox) convert NO2− and NH4+ to N2 using an enzyme called hydrazine oxidoreductase. Genomic studies conducted in these ecosystems reveal a growing abundance of the genes encoding for the proteins responsible for the dissimilatory nitrate reduction to ammonium (DNRA) and anammox at the core of these OMZs. [12] Such studies provide information to map out the nitrogen cycle and demystify missing links and unexplored pathways in the water column. [13] Anammox is often coupled to denitrification as a source of NH4+ in OMZs or to DNRA in sediments. [7] [6] DNRA has been found to be the dominant process supplying NH4+ near the shelf and upper slope of sediments because of the presence of large bacterial mats made up of the giant sulfur-oxidizing bacteria Thioploca spp. and Beggiatoa spp. which reduce NO3− and/or NO2− to NH4+ using reduced sulfur. [7] [14] Denitrification and anammox account for about 30-50% of the N losses in OMZs, where the total N loss determined by the supply of sinking organic matter available. [15] [16] [6]

Additionally, ammonium and nitrite oxidation are key processes in N cycling in anoxic environments. Ammonium oxidation is the first step in nitrification and ammonia-oxidizing bacteria (AOB) converts NH3 to NO2−. [6] Followed by nitrite oxidation by nitrite-oxidizing bacteria (NOB), which converts NO2− to NO3−. [6] Ammonium and nitrite oxidizers have a high affinity for O2 and can use nanomolar concentrations of O2 to oxidize ammonium and nitrite. [17] These small concentrations of O2 can be supplied by photosynthesis by Prochlorococcus spp. [18] or by horizontal mixing by jets and eddies. [19] In anoxic environments, the competition between ammonium and nitrite oxidization and anammox and denitrification for ammonium and nitrite play an important role in controlling nitrogen loss in OMZs. [17]

Sources of ammonium for anammox bacteria

Anaerobic ammonium oxidation with nitrite (anammox) is a major pathway of fixed nitrogen removal in the anoxic zones of the open ocean. [20] Anammox requires a source of ammonium, which under anoxic conditions could be supplied by the breakdown of sinking organic matter via heterotrophic denitrification. However, at many locations where anammox is observed, denitrification rates are small or undetectable. [21] Alternative sources of NH4+ than denitrification, such as the DNRA, the diffusion and advection from sulfate-reducing sediments, or from microaerobic remineralization at the boundaries of anoxic waters, can supply NH4+ to anammox bacterial communities, [22] even though it is not yet clear how much they can influence the process. [22] [23] Another source of NH4+, which plays an important role in the N cycle of OMZs by contributing to the decoupling of anammox and denitrification, is the excretion of NH4+ by diel vertically migrating animals. To escape predation, diel vertical migration (DVM) of zooplankton and micronekton can reach the anoxic layers of the major OMZs of the open ocean, and because animals excrete reduced N mostly as NH4+, they can fuel anammox directly and decouple it from denitrification. The downward export of organic matter by migrating zooplankton and micronekton is generally smaller than that of particles at the base of the euphotic zone. [24] However, sinking particles are rapidly consumed with depth, and the active transport by migrators can exceed particle remineralization in deeper layers where animals congregate during the daytime. [24] As a result, inside anoxic waters the excretion of NH4+ by vertically migrating animals could alter the balance between fixed N removal pathways, decoupling anammox and denitrification and enhancing anammox above the values predicted by typical stoichiometry. [24]

Methanogenesis cycle with intermediates Methanogenesis cycle.png
Methanogenesis cycle with intermediates

Methanogenesis

Sulfate reduction pathway Dissimilatory sulfate reduction.svg
Sulfate reduction pathway

Methanogenesis is the process by which methanogen microbes form methane (CH4). OMZs are known to contain the largest amount of methane in the open ocean. [25] Methanogens can also oxidize methane as they have the genes to do so, however this requires oxygen which they obtain from photosynthetic organisms in the upper anoxic zone. [25] Ciliates may also aid methanogens through symbiosis to help facilitate methanogenesis. [26] As ciliates have hydrogenosomes, which release hydrogen molecules under low oxygen conditions, they have the ability to host endosymbiotic methanogens. [27]

Sulfate Reduction

Sulfate reduction, which occurs with the help of sulfate-reducing microorganisms, is used in the cryptic sulfur cycle. This cycle is continuous oxidation and reduction of sulfate and uses sulfate as the terminal electron acceptor rather than oxygen. The cycle was purposed to help contribute to the energy flow to anoxic water off the coast of Chile. [28]

Aerobic Microbial Respiration

Aerobic organisms require oxygen to survive and as oxygen becomes limited in OMZs bacteria begin to use other molecules to oxidize organic matter such as nitrate. [29] Aerobic respiration in OMZs helps remineralize organic matter and is a major source of ammonium for most of the upper oxygen minimal zones. [30] It was also found that bacteria from OMZs use a 1/6 of the oxygen for respiration compared bacteria in normal waters. [31]

Changes due to climate change

This section is an excerpt from Ocean deoxygenation § Role of climate change.[ edit ]

While oxygen minimum zones (OMZs) occur naturally, they can be exacerbated by human impacts like climate change and land-based pollution from agriculture and sewage. The prediction of current climate models and climate change scenarios is that substantial warming and loss of oxygen throughout the majority of the upper ocean will occur. [32] Global warming increases ocean temperatures, especially in shallow coastal areas. When the water temperature increases, its ability to hold oxygen decreases, leading to oxygen concentrations going down in the water. [33] This compounds the effects of eutrophication in coastal zones described above.

Open ocean areas with no oxygen have grown more than 1.7 million square miles in the last 50 years, and coastal waters have seen a tenfold increase in low-oxygen areas in the same time. [34]

Measurement of dissolved oxygen in coastal and open ocean waters for the past 50 years has revealed a marked decline in oxygen content. [35] [36] [37] This decline is associated with expanding spatial extent, expanding vertical extent, and prolonged duration of oxygen-poor conditions in all regions of the global oceans. Examinations of the spatial extent of OMZs in the past through paleoceanographical methods clearly shows that the spatial extent of OMZs has expanded through time, and this expansion is coupled to ocean warming and reduced ventilation of thermocline waters. [38]

Research has attempted to model potential changes to OMZs as a result of rising global temperatures and human impact. This is challenging due to the many factors that could contribute to changes in OMZs. [39] The factors used for modeling change in OMZs are numerous, and in some cases hard to measure or quantify. [40] Some of the processes being studied are changes in oxygen gas solubility as a result of rising ocean temperatures, as well as changes in the amount of respiration and photosynthesis occurring around OMZs. [41] Many studies have concluded that OMZs are expanding in multiple locations, but fluctuations of modern OMZs are still not fully understood. [41] [40] [42] Existing Earth system models project considerable reductions in oxygen and other physical-chemical variables in the ocean due to climate change, with potential ramifications for ecosystems and humans.

The global decrease in oceanic oxygen content is statistically significant and emerging beyond the envelope of natural fluctuations. [35] This trend of oxygen loss is accelerating, with widespread and obvious losses occurring after the 1980s. [43] [35] The rate and total content of oxygen loss varies by region, with the North Pacific emerging as a particular hotspot of deoxygenation due to the increased amount of time since its deep waters were last ventilated (see thermohaline circulation) and related high apparent oxygen utilization (AOU). [35] [36] Estimates of total oxygen loss in the global ocean range from 119 to 680 T mol decade−1 since the 1950s. [35] [36] These estimates represent 2% of the global ocean oxygen inventory. [37]

Melting of gas hydrates in bottom layers of water may result in the release of more methane from sediments and subsequent consumption of oxygen by aerobic respiration of methane to carbon dioxide. Another effect of climate change on oceans that causes ocean deoxygenation is circulation changes. As the ocean warms from the surface, stratification is expected to increase, which shows a tendency for slowing down ocean circulation, which then increases ocean deoxygenation. [44]

See also

Related Research Articles

<span class="mw-page-title-main">Nitrogen cycle</span> Biogeochemical cycle by which nitrogen is converted into various chemical forms

The nitrogen cycle is the biogeochemical cycle by which nitrogen is converted into multiple chemical forms as it circulates among atmospheric, terrestrial, and marine ecosystems. The conversion of nitrogen can be carried out through both biological and physical processes. Important processes in the nitrogen cycle include fixation, ammonification, nitrification, and denitrification. The majority of Earth's atmosphere (78%) is atmospheric nitrogen, making it the largest source of nitrogen. However, atmospheric nitrogen has limited availability for biological use, leading to a scarcity of usable nitrogen in many types of ecosystems.

<span class="mw-page-title-main">Nitrification</span> Biological oxidation of ammonia/ammonium to nitrate

Nitrification is the biological oxidation of ammonia to nitrate via the intermediary nitrite. Nitrification is an important step in the nitrogen cycle in soil. The process of complete nitrification may occur through separate organisms or entirely within one organism, as in comammox bacteria. The transformation of ammonia to nitrite is usually the rate limiting step of nitrification. Nitrification is an aerobic process performed by small groups of autotrophic bacteria and archaea.

Anaerobic respiration is respiration using electron acceptors other than molecular oxygen (O2). Although oxygen is not the final electron acceptor, the process still uses a respiratory electron transport chain.

<span class="mw-page-title-main">Denitrification</span> Microbially facilitated process

Denitrification is a microbially facilitated process where nitrate (NO3−) is reduced and ultimately produces molecular nitrogen (N2) through a series of intermediate gaseous nitrogen oxide products. Facultative anaerobic bacteria perform denitrification as a type of respiration that reduces oxidized forms of nitrogen in response to the oxidation of an electron donor such as organic matter. The preferred nitrogen electron acceptors in order of most to least thermodynamically favorable include nitrate (NO3−), nitrite (NO2−), nitric oxide (NO), nitrous oxide (N2O) finally resulting in the production of dinitrogen (N2) completing the nitrogen cycle. Denitrifying microbes require a very low oxygen concentration of less than 10%, as well as organic C for energy. Since denitrification can remove NO3−, reducing its leaching to groundwater, it can be strategically used to treat sewage or animal residues of high nitrogen content. Denitrification can leak N2O, which is an ozone-depleting substance and a greenhouse gas that can have a considerable influence on global warming.

The mesopelagiczone, also known as the middle pelagic or twilight zone, is the part of the pelagic zone that lies between the photic epipelagic and the aphotic bathypelagic zones. It is defined by light, and begins at the depth where only 1% of incident light reaches and ends where there is no light; the depths of this zone are between approximately 200 to 1,000 meters below the ocean surface.

The oxygen minimum zone (OMZ), sometimes referred to as the shadow zone, is the zone in which oxygen saturation in seawater in the ocean is at its lowest. This zone occurs at depths of about 200 to 1,500 m (700–4,900 ft), depending on local circumstances. OMZs are found worldwide, typically along the western coast of continents, in areas where an interplay of physical and biological processes concurrently lower the oxygen concentration and restrict the water from mixing with surrounding waters, creating a "pool" of water where oxygen concentrations fall from the normal range of 4–6 mg/L to below 2 mg/L.

<span class="mw-page-title-main">Anammox</span> Anaerobic ammonium oxidation, a microbial process of the nitrogen cycle

Anammox, an abbreviation for "anaerobic ammonium oxidation", is a globally important microbial process of the nitrogen cycle that takes place in many natural environments. The bacteria mediating this process were identified in 1999, and were a great surprise for the scientific community. In the anammox reaction, nitrite and ammonium ions are converted directly into diatomic nitrogen and water.

<span class="mw-page-title-main">Sediment–water interface</span> The boundary between bed sediment and the overlying water column

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f-ratio (oceanography) In oceanic biogeochemistry, the fraction of total primary production fuelled by nitrate

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Microbial metabolism is the means by which a microbe obtains the energy and nutrients it needs to live and reproduce. Microbes use many different types of metabolic strategies and species can often be differentiated from each other based on metabolic characteristics. The specific metabolic properties of a microbe are the major factors in determining that microbe's ecological niche, and often allow for that microbe to be useful in industrial processes or responsible for biogeochemical cycles.

<span class="mw-page-title-main">Lithoautotroph</span>

A lithoautotroph is an organism which derives energy from reactions of reduced compounds of mineral (inorganic) origin. Two types of lithoautotrophs are distinguished by their energy source; photolithoautotrophs derive their energy from light while chemolithoautotrophs (chemolithotrophs or chemoautotrophs) derive their energy from chemical reactions. Chemolithoautotrophs are exclusively microbes. Photolithoautotrophs include macroflora such as plants; these do not possess the ability to use mineral sources of reduced compounds for energy. Most chemolithoautotrophs belong to the domain Bacteria, while some belong to the domain Archaea. Lithoautotrophic bacteria can only use inorganic molecules as substrates in their energy-releasing reactions. The term "lithotroph" is from Greek lithos (λίθος) meaning "rock" and trōphos (τροφοσ) meaning "consumer"; literally, it may be read "eaters of rock". The "lithotroph" part of the name refers to the fact that these organisms use inorganic elements/compounds as their electron source, while the "autotroph" part of the name refers to their carbon source being CO2. Many lithoautotrophs are extremophiles, but this is not universally so, and some can be found to be the cause of acid mine drainage.

Nitrifying bacteria are chemolithotrophic organisms that include species of genera such as Nitrosomonas, Nitrosococcus, Nitrobacter, Nitrospina, Nitrospira and Nitrococcus. These bacteria get their energy from the oxidation of inorganic nitrogen compounds. Types include ammonia-oxidizing bacteria (AOB) and nitrite-oxidizing bacteria (NOB). Many species of nitrifying bacteria have complex internal membrane systems that are the location for key enzymes in nitrification: ammonia monooxygenase, hydroxylamine oxidoreductase, and nitrite oxidoreductase.

<span class="mw-page-title-main">Ocean deoxygenation</span> Reduction of the oxygen content of the oceans

Ocean deoxygenation is the reduction of the oxygen content in different parts of the ocean due to human activities. It occurs firstly in coastal zones where eutrophication has driven some quite rapid declines in oxygen to very low levels. This type of ocean deoxygenation is also called "dead zones". Secondly, there is now an ongoing reduction in oxygen levels in the open ocean: naturally occurring low oxygen areas are now expanding slowly. This expansion is happening as a consequence of human caused climate change. The resulting decrease in oxygen content of the oceans poses a threat to marine life, as well as to people who depend on marine life for nutrition or livelihood. Ocean deoxygenation poses implications for ocean productivity, nutrient cycling, carbon cycling, and marine habitats.

<span class="mw-page-title-main">Bacterioplankton</span> Bacterial component of the plankton that drifts in the water column

Bacterioplankton refers to the bacterial component of the plankton that drifts in the water column. The name comes from the Ancient Greek word πλανκτος, meaning "wanderer" or "drifter", and bacterium, a Latin term coined in the 19th century by Christian Gottfried Ehrenberg. They are found in both seawater and freshwater.

<span class="mw-page-title-main">SHARON Wastewater Treatment</span>

SHARON is a sewage treatment process. A partial nitrification process of sewage treatment used for the removal of ammonia and organic nitrogen components from wastewater flow streams. The process results in stable nitrite formation, rather than complete oxidation to nitrate. Nitrate formation by nitrite oxidising bacteria (NOB) is prevented by adjusting temperature, pH, and retention time to select for nitrifying ammonia oxidising bacteria (AOB). Denitrification of waste streams utilizing SHARON reactors can proceed with an anoxic reduction, such as anammox.

CandidatusScalindua wagneri is a Gram-negative coccoid-shaped bacterium that was first isolated from a wastewater treatment plant. This bacterium is an obligate anaerobic chemolithotroph that undergoes anaerobic ammonium oxidation (anammox). It can be used in the wastewater treatment industry in nitrogen reactors to remove nitrogenous wastes from wastewater without contributing to fixed nitrogen loss and greenhouse gas emission.

"Candidatus Scalindua" is a bacterial genus, and a proposed member of the order Planctomycetales. These bacteria lack peptidoglycan in their cell wall and have a compartmentalized cytoplasm. They are ammonium oxidizing bacteria found in marine environments.

Dissimilatory nitrate reduction to ammonium (DNRA), also known as nitrate/nitrite ammonification, is the result of anaerobic respiration by chemoorganoheterotrophic microbes using nitrate (NO3−) as an electron acceptor for respiration. In anaerobic conditions microbes which undertake DNRA oxidise organic matter and use nitrate (rather than oxygen) as an electron acceptor, reducing it to nitrite, then ammonium (NO3−→NO2−→NH4+).

Anammox is a wastewater treatment technique that removes nitrogen using anaerobic ammonium oxidation (anammox). This process is performed by anammox bacteria which are autotrophic, meaning they do not need organic carbon for their metabolism to function. Instead, the metabolism of anammox bacteria convert ammonium and nitrite into dinitrogen gas. Anammox bacteria are a wastewater treatment technique and wastewater treatment facilities are in the process of implementing anammox-based technologies to further enhance ammonia and nitrogen removal.

References

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