Microbiology of oxygen minimum zones

File:OMZ cycles.jpg

Biological productivity (photosynthesis) in marine ecosystems is often limited by the bioavailability of nitrogen.{{cite journal |last1=Pajares |first1=S |last2=Ramos |first2=R |title=Processes and Microorganisms Involved in the Marine Nitrogen Cycle: Knowledge and Gaps |journal=Frontiers in Marine Science |date=2019 |volume=6 |pages=739 |doi=10.3389/fmars.2019.00739|doi-access=free }} 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.{{cite journal |last1=Bohlen |first1=L |last2=Dale |first2=AW |last3=Sommer |first3=S |last4=Mosch |first4=T |last5=Hensen |first5=C |last6=Noffke |first6=A |last7=Scholz |first7=F |last8=Wallmann |first8=K |title=Benthic nitrogen cycling traversing the Peruvian oxygen minimum zone |journal=Geochimica et Cosmochimica Acta |date=2011 |volume=75 |issue=20 |pages=6095–6111|doi=10.1016/j.gca.2011.08.010 |url=http://oceanrep.geomar.de/12030/1/Bohlen_et_al_2011.pdf }} 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.{{cite journal |last1=Kirkpatrick |first1=J |last2=Fuchsman |first2=C |last3=Yakushev |first3=E |last4=Egorov |first4=A |last5=Staley |first5=J |last6=Murray |first6=J |title=Dark N2 fixation: nifH expression in the redoxcline of the Black Sea |journal=Aquatic Microbial Ecology |date=2018 |volume=82 |pages=43–58|doi=10.3354/ame01882 |hdl=11250/2597363 |s2cid=56444453 |hdl-access=free }} 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).{{cite web |url=http://omz.microbiology.ubc.ca/page9/index.html |website=OMZ Microbes - A SCOR working group|title=Objectives}} Heterotrophic denitrification is a multi-step process that uses organic matter to reduce NO₃⁻ to N₂ in oxygen-depleted environments like OMZs and sediments. 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.{{cite journal |last1=Ganesh |first1=S |last2=Parris |first2=DJ |last3=DeLong |first3=EF |last4=Stewart |first4=FJ |title=Metagenomic analysis of size-fractionated picoplankton in a marine oxygen minimum zone. |journal=ISME Journal |date=2014 |volume=8 |issue=1 |pages=187–211|doi=10.1038/ismej.2013.144 |pmid=24030599 |pmc=3869020 }}{{cite journal |last1=Fuchsman |first1=CA |last2=Devol |first2=AH |last3=Saunders |first3=JK |last4=McKay |first4=C |last5=Rocap |first5=G |title=Niche Partitioning of the N Cycling Microbial Community of an Offshore Oxygen Deficient Zone |journal=Frontiers in Microbiology |date=2017 |volume=8 |pages=2384|doi=10.3389/fmicb.2017.02384 |pmid=29259587 |pmc=5723336 |doi-access=free }} 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.{{cite web |title=How nutrients are removed in oxygen-depleted regions of the ocean |url=https://www.uni-kiel.de/en/details/news/how-nutrients-are-removed-in-oxygen-depleted-regions-of-the-ocean/|date=2018-11-22|archive-url=https://web.archive.org/web/20181127110250/https://www.uni-kiel.de/en/details/news/how-nutrients-are-removed-in-oxygen-depleted-regions-of-the-ocean/|archive-date=2018-11-27}} Such studies provide information to map out the nitrogen cycle and demystify missing links and unexplored pathways in the water column.{{cite journal |last1=Ulloa, Canfield, DeLong, Letelier, Stewart |first1=Osvaldo, Donald E. ,Edward F.,Ricardo M., Frank J. |title=Microbial oceanography of anoxic oxygen minimum zones |journal=Proceedings of the National Academy of Sciences |volume=109 |issue=40 |pages=15996–16003 |date=October 2, 2012 |doi=10.1073/pnas.1205009109|pmid=22967509 |pmc=3479542 |bibcode=2012PNAS..10915996U |doi-access=free }} Anammox is often coupled to denitrification as a source of NH₄⁺ in OMZs or to DNRA in sediments. 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.{{cite journal |last1=Dale |first1=AW |last2=Sommer |first2=S |last3=Lomnitz |first3=U |last4=Bourbonnais |first4=A |last5=Wallmann |first5=K |title=Biological nitrate transport in sediments on the Peruvian margin mitigates benthic sulfide emissions and drives pelagic N loss during stagnation events |journal=Deep Sea Research Part I: Oceanographic Research Papers |date=2016 |volume=112 |pages=123–136|doi=10.1016/j.dsr.2016.02.013 |bibcode=2016DSRI..112..123D |url=http://oceanrep.geomar.de/31809/1/Dale.pdf }} 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.{{cite journal |last1=Babbin |first1=AR |last2=Keil |first2=RG |last3=Devol |first3=AH |last4=Ward |first4=BB |title=Organic Matter Stoichiometry, Flux, and Oxygen Control Nitrogen Loss in the Ocean |journal=Science |date=2014 |volume=344 |issue=6182 |pages=406–408|doi=10.1126/science.1248364 |pmid=24763588 |bibcode=2014Sci...344..406B |s2cid=206553608 |doi-access=free }}{{cite journal |last1=Kalvelage |first1=T |last2=Lavik |first2=G |last3=Lam |first3=P |last4=Contreras |first4=S |last5=Arteaga |first5=L |last6=Löscher |first6=CR |last7=Oschiles |first7=A |last8=Paulmier |first8=A |last9=Stramma |first9=L |last10=Kuypers |first10=MMM |title=Nitrogen cycling driven by organic matter export in the South Pacific oxygen minimum zone |journal=Nature Geoscience |date=2013 |volume=6 |issue=3 |pages=228–234|doi=10.1038/ngeo1739 |bibcode=2013NatGe...6..228K |url=https://hal.archives-ouvertes.fr/hal-00998635/file/9755_2_merged_1358171649.pdf }}

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⁻. Followed by nitrite oxidation by nitrite-oxidizing bacteria (NOB), which converts NO₂⁻ to NO₃⁻. Ammonium and nitrite oxidizers have a high affinity for O₂ and can use nanomolar concentrations of O₂ to oxidize ammonium and nitrite.{{cite journal |last1=Bristow |first1=LA |last2=Dalsgaard |first2=T |last3=Tiano |first3=L |last4=Mills |first4=DB |last5=Bertagnolli |first5=AD |last6=Wright |first6=JJ |last7=Hallam |first7=SJ |last8=Ulloa |first8=O |last9=Canfield |first9=DE |last10=Revsbech |first10=NP |display-authors=etal |title=Ammonium and nitrite oxidation at nanomolar oxygen concentrations in oxygen minimum zone waters |journal=Proceedings of the National Academy of Sciences |date=2016 |volume=113 |issue=38 |pages=10601–10606|doi=10.1073/pnas.1600359113 |pmid=27601665 |pmc=5035861 |bibcode=2016PNAS..11310601B |doi-access=free }} These small concentrations of O₂ can be supplied by photosynthesis by Prochlorococcus spp.{{cite journal |last1=Garcia-Robledo |first1=E |last2=Padilla |first2=CC |last3=Aldunate |first3=M |last4=Stewart |first4=FJ |last5=Ulloa |first5=O |last6=Paulmier |first6=A |last7=Gregori |first7=G |last8=Revsbech |first8=NP |title=Cryptic oxygen cycling in anoxic marine zones |journal=Proceedings of the National Academy of Sciences |date=2017 |volume=114 |issue=31 |pages=8319–8324|doi=10.1073/pnas.1619844114 |pmid=28716941 |pmc=5547588 |bibcode=2017PNAS..114.8319G |doi-access=free }} or by horizontal mixing by jets and eddies.{{cite journal |last1=Margolskee |first1=J |last2=Fuchsman |first2=C |last3=Yakushev |first3=E |last4=Egorov |first4=A |last5=Staley |first5=J |last6=Murray |first6=J |title=Dark N2 fixation: nifH expression in the redoxcline of the Black Sea |journal=Global Biogeochemical Cycles |date=2019 |volume=33 |pages=875–890|doi=10.1029/2018GB006149 |doi-access=free }} 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.

Anaerobic ammonium oxidation with nitrite (anammox) is a major pathway of fixed nitrogen removal in the anoxic zones of the open ocean.{{cite journal |last1=DeVries |first1=T |last2=Deutsch |first2=C |last3=Primeau |first3=F |last4=Chang |first4=B |last5=Devol |first5=A |title=Global rates of water-column denitrification derived from nitrogen gas measurements |journal=Nature Geoscience |date=2012 |volume=5 |issue=8 |pages=547–550|doi=10.1038/ngeo1515 |bibcode=2012NatGe...5..547D |url=https://escholarship.org/uc/item/6xg6x5vc }} 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.{{cite journal |last1=Dalsgaard |first1=T |last2=Thamdrup |first2=B |last3=Farías |first3=L |last4=Revsbech |first4=NP |title=Anammox and denitrification in the oxygen minimum zone of the eastern South Pacific |journal=Limnology and Oceanography |date=2012 |volume=57 |issue=5 |pages=1331–1346|doi=10.4319/lo.2012.57.5.1331 |bibcode=2012LimOc..57.1331D |s2cid=53395710 |url=https://pure.au.dk/ws/files/47778236/Dalsgaard_et_al_Limnol_Oceanogr_2012_Anammox_and_denitrification_in_the_oxygen_minimum_zone_of_the_eastern_South_Pacific.pdf }} 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,{{cite journal |last1=Lam |first1=P |display-authors=etal |title=Revising the nitrogen cycle in the Peruvian oxygen minimum zone |journal=Proceedings of the National Academy of Sciences |date=2009 |volume=106 |issue=12 |pages=4752–4757|doi=10.1073/pnas.0812444106 |pmid=19255441 |pmc=2649953 |bibcode=2009PNAS..106.4752L |doi-access=free }} even though it is not yet clear how much they can influence the process.{{cite journal |last1=Lam |first1=P |last2=Kuypers |first2=MM |title=Microbial nitrogen cycling processes in oxygen minimum zones |journal= Annual Review of Marine Science|date=2011 |volume=3 |pages=317–345|doi=10.1146/annurev-marine-120709-142814 |pmid=21329208 |bibcode=2011ARMS....3..317L |hdl=21.11116/0000-0001-CA25-2 |hdl-access=free }} 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.{{cite journal |last1=Bianchi |first1=D |last2=Babbin |first2=AR |last3=Galbraith |first3=ED |title=Enhancement of anammox by the excretion of diel vertical migrators |journal=Proceedings of the National Academy of Sciences |date=2014 |volume=111 |issue=44 |pages=15653–15658|doi=10.1073/pnas.1410790111 |pmid=25288743 |pmc=4226083 |bibcode=2014PNAS..11115653B |doi-access=free }} 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. 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.

File:Methanogenesis cycle.png

File:Dissimilatory sulfate reduction.svg

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.{{Cite journal|last1=Bertagnolli|first1=Anthony D.|last2=Stewart|first2=Frank J.|date=2018-09-24|title=Microbial niches in marine oxygen minimum zones|journal=Nature Reviews Microbiology|volume=16|issue=12|pages=723–729|language=En|doi=10.1038/s41579-018-0087-z|pmid=30250271|s2cid=52811177|issn=1740-1526}} 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. Ciliates may also aid methanogens through symbiosis to help facilitate methanogenesis.{{Cite journal|last1=Orsi|first1=William|last2=Song|first2=Young C|last3=Hallam|first3=Steven|last4=Edgcomb|first4=Virginia|date=2012-03-08|title=Effect of oxygen minimum zone formation on communities of marine protists|journal=The ISME Journal|language=En|volume=6|issue=8|pages=1586–1601|doi=10.1038/ismej.2012.7|pmid=22402396|pmc=3400406|issn=1751-7362}} As ciliates have hydrogenosomes, which release hydrogen molecules under low oxygen conditions, they have the ability to host endosymbiotic methanogens.{{Citation|last1=Hackstein|first1=Johannes H. P.|title=Anaerobic Ciliates and Their Methanogenic Endosymbionts|date=2018|work=(Endo)symbiotic Methanogenic Archaea|pages=13–23|publisher=Springer International Publishing|language=en|doi=10.1007/978-3-319-98836-8_2|isbn=9783319988351|last2=de Graaf|first2=Rob M.}}

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.{{Cite journal|last1=Canfield|first1=Don E.|last2=Stewart|first2=Frank J.|last3=Thamdrup|first3=Bo|last4=Brabandere|first4=Loreto De|last5=Dalsgaard|first5=Tage|last6=Delong|first6=Edward F.|last7=Revsbech|first7=Niels Peter|last8=Ulloa|first8=Osvaldo|date=2010-12-03|title=A Cryptic Sulfur Cycle in Oxygen-Minimum–Zone Waters off the Chilean Coast|journal=Science|language=en|volume=330|issue=6009|pages=1375–1378|doi=10.1126/science.1196889|issn=0036-8075|pmid=21071631|bibcode=2010Sci...330.1375C|hdl=1721.1/108425|s2cid=39178420|url=https://dspace.mit.edu/bitstream/1721.1/108425/1/Canfield_Science_330_1375_2010.pdf|hdl-access=free}}

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.{{Cite journal|last1=Kalvelage|first1=Tim|last2=Lavik|first2=Gaute|last3=Jensen|first3=Marlene M.|last4=Revsbech|first4=Niels Peter|last5=Löscher|first5=Carolin|last6=Schunck|first6=Harald|last7=Desai|first7=Dhwani K.|last8=Hauss|first8=Helena|last9=Kiko|first9=Rainer|date=2015-07-20|title=Aerobic Microbial Respiration In Oceanic Oxygen Minimum Zones|journal=PLOS ONE|language=en|volume=10|issue=7|pages=e0133526|doi=10.1371/journal.pone.0133526|issn=1932-6203|pmc=4507870|pmid=26192623|bibcode=2015PLoSO..1033526K|doi-access=free}} Aerobic respiration in OMZs helps remineralize organic matter and is a major source of ammonium for most of the upper oxygen minimal zones.{{Cite journal|last1=Kalvelage|first1=Tim|last2=Lavik|first2=Gaute|last3=Jensen|first3=Marlene M.|last4=Revsbech|first4=Niels Peter|last5=Löscher|first5=Carolin|last6=Schunck|first6=Harald|last7=Desai|first7=Dhwani K.|last8=Hauss|first8=Helena|last9=Kiko|first9=Rainer|date=2015-07-20|title=Aerobic Microbial Respiration In Oceanic Oxygen Minimum Zones|journal=PLOS ONE|volume=10|issue=7|pages=e0133526|doi=10.1371/journal.pone.0133526|issn=1932-6203|pmc=4507870|pmid=26192623|bibcode=2015PLoSO..1033526K|doi-access=free}} It was also found that bacteria from OMZs use a 1/6 of the oxygen for respiration compared bacteria in normal waters.{{Cite journal|last1=Ulloa|first1=Osvaldo|last2=Canfield|first2=Donald E.|last3=DeLong|first3=Edward F.|last4=Letelier|first4=Ricardo M.|last5=Stewart|first5=Frank J.|date=2012-10-02|title=Microbial oceanography of anoxic oxygen minimum zones|journal=Proceedings of the National Academy of Sciences|language=en|volume=109|issue=40|pages=15996–16003|doi=10.1073/pnas.1205009109|issn=0027-8424|pmc=3479542|pmid=22967509|bibcode=2012PNAS..10915996U|doi-access=free}}

{{excerpt|Ocean deoxygenation#Role of climate change}}

• Ocean deoxygenation
• Anoxic event
• Anoxic waters
• Dead zone (ecology)
• Ocean acidification

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Category:Environmental microbiology

Category:Biological oceanography