Citation: | WANG Yan-tao, CHEN Quan-rui, MING Hong-xia, SONG Lin-sheng, FAN Jing-feng. Research advances in microbial effects in marine oxygen minimum zones[J]. Chinese Journal of MARINE ENVIRONMENTAL SCIENCE, 2020, 39(2): 321-328. DOI: 10.12111/j.mes20200223 |
Oxygen Minimum Zones (OMZs) were special habitats with very low dissolved oxygen content in the ocean.They were widely distributed in oceans or offshore areas around the world.Low level oxygen could damage ecosystem functions and affect economic development along the coast.In severe cases, they could lead to species extinction.Due to the low oxygen, there was almost no multicellular organism in the region, the internal elemental circulation was almost driven by microorganisms entirely, so the position of microorganisms was crucial.This paper first briefly described the formation mechanism of OMZs and the factors affected the formation and development of them, and then reviewed the unique respiratory patterns of microbes in order to adapt to the environmental change.The most direct impact of OMZs on microorganisms was that they formed community structures and functional activities different from the oxygen-rich environment, and this part was summarized as microbial effects.The study of microorganisms in OMZs was complex and challenging, at the same time, it provided a special way for us to understand the adaptability, diversity and evolution of microorganisms in the environment better.It had a great significance to improve our understanding of biogeochemical cycle.
[1] |
GUO Y R, RONG Z R, LI B, et al.Physical processes causing the formation of hypoxia off the Changjiang estuary after Typhoon Chan-hom, 2015[J].Journal of Oceanology and Limnology, 2019, 37(1):1-17. doi: 10.1007/s00343-019-7336-5
|
[2] |
LAM P, KUYPERS M M M.Microbial nitrogen cycling processes in oxygen minimum zones[J].Annual Review of Marine Science, 2011, 3:317-345. doi: 10.1146/annurev-marine-120709-142814
|
[3] |
DIAZ R J, ROSENBERG R.Spreading dead zones and consequences for marine ecosystems[J].Science, 2008, 321(5891):926-929. doi: 10.1126/science.1156401
|
[4] |
PENG X F, FUCHSMAN C A, JAYAKUMAR A, et al.Ammonia and nitrite oxidation in the Eastern Tropical North Pacific[J].Global Biogeochemical Cycles, 2015, 29(12):2034-2049. doi: 10.1002/2015GB005278
|
[5] |
WIGNALL P B, TWITCHETT R J.Oceanic anoxia and the end Permian mass extinction[J].Science, 1996, 272(5265):1155-1158. doi: 10.1126/science.272.5265.1155
|
[6] |
BENTON M J, TWITCHETT R J.How to kill (almost) all life:the end-Permian extinction event[J].Trends in Ecology & Evolution, 2003, 18(7):358-365. http://www.sciencedirect.com/science/article/pii/S0169534703000934
|
[7] |
STRAMMA L, JOHNSON G C, SPRINTALL J, et al.Expanding oxygen-minimum zones in the tropical oceans[J].Science, 2008, 320(5876):655-658. doi: 10.1126/science.1153847
|
[8] |
SARMA V V S S, UDAYA BHASKAR T V S.Ventilation of oxygen to oxygen minimum zone due to anticyclonic eddies in the bay of bengal[J].Journal of Geophysical Research:Biogeosciences, 2018, 123(7):2145-2153. doi: 10.1029/2018JG004447
|
[9] |
SANTOS G C, KERR R, AZEVEDO J L L, et al.Influence of Antarctic intermediate water on the deoxygenation of the Atlantic Ocean[J].Dynamics of Atmospheres and Oceans, 2016, 76:72-82. doi: 10.1016/j.dynatmoce.2016.09.002
|
[10] |
BEVER A J, FRIEDRICHS M A M, FRIEDRICHS C T, et al.Estimating hypoxic volume in the Chesapeake bay using two continuously sampled oxygen profiles[J].Journal of Geophysical Research, 2018, 123(9):6392-6407. http://www.wanfangdata.com.cn/details/detail.do?_type=perio&id=10.1029/2018JC014129
|
[11] |
ZILLÉN L, CONLEY D J, ANDRÉN T, et al.Past occurrences of hypoxia in the Baltic Sea and the role of climate variability, environmental change and human impact[J].Earth-Science Reviews, 2008, 91(1/2/3/4):77-92. http://www.wanfangdata.com.cn/details/detail.do?_type=perio&id=16d674ba9f5c84562f7a8fecceedd42a
|
[12] |
PITCHER A, VILLANUEVA L, HOPMANS E C, et al.Niche segregation of ammonia-oxidizing archaea and anammox bacteria in the Arabian Sea oxygen minimum zone[J].The ISME Journal, 2011, 5(12):1896-1904. doi: 10.1038/ismej.2011.60
|
[13] |
ZHAI W D, ZHAO H D, ZHENG N, et al.Coastal acidification in summer bottom oxygen-depleted waters in northwestern-northern Bohai Sea from June to August in 2011[J].Chinese Science Bulletin, 2012, 57(9):1062-1068. doi: 10.1007/s11434-011-4949-2
|
[14] |
QIAN W, GAN J P, LIU J W, et al.Current status of emerging hypoxia in a eutrophic estuary:the lower reach of the Pearl River Estuary, China[J].Estuarine, Coastal and Shelf Science, 2018, 205:58-67. doi: 10.1016/j.ecss.2018.03.004
|
[15] |
SU J Z, DAI M H, HE B Y, et al.Tracing the origin of the oxygen-consuming organic matter in the hypoxic zone in a large eutrophic estuary:the lower reach of the Pearl River Estuary, China[J].Biogeosciences Discussions, 2017, 14(18):4085-4099. doi: 10.5194/bg-14-4085-2017
|
[16] |
LÜKE C, SPETH D R, KOX M A R, et al.Metagenomic analysis of nitrogen and methane cycling in the Arabian Sea oxygen minimum zone[J].PeerJ, 2016, 4:e1924. doi: 10.7717/peerj.1924
|
[17] |
HELLY J J, LEVIN L A.Global distribution of naturally occurring marine hypoxia on continental margins[J].Deep Sea Research Part Ⅰ:Oceanographic Research Papers, 2004, 51(9):1159-1168. doi: 10.1016/j.dsr.2004.03.009
|
[18] |
LÖSCHER C R, KOCK A, KÖNNEKE M, et al.Production of oceanic nitrous oxide by ammonia-oxidizing archaea[J].Biogeosciences, 2012, 9(7):2419-2429. doi: 10.5194/bg-9-2419-2012
|
[19] |
HALLAM S J, TORRES-BELTRÁN M, HAWLEY A K.Monitoring microbial responses to ocean deoxygenation in a model oxygen minimum zone[J].Scientific Data, 2017, 4:170158. doi: 10.1038/sdata.2017.158
|
[20] |
MARTINEZ-REY J, BOPP L, GEHLEN M, et al.Projections of oceanic N2O emissions in the 21st century using the IPSL Earth system model[J].Biogeosciences, 2015, 12(13):4133-4148. doi: 10.5194/bg-12-4133-2015
|
[21] |
PAULMIER A, RUIZ-PINO D, GARCON V.The oxygen minimum zone (OMZ) off Chile as intense source of CO2 and N2O[J].Continental Shelf Research, 2008, 28(20):2746-2756. doi: 10.1016/j.csr.2008.09.012
|
[22] |
SCHMIDTKO S, STRAMMA L, VISBECK M.Decline in global oceanic oxygen content during the past five decades[J].Nature, 2017, 542(7641):335-339. doi: 10.1038/nature21399
|
[23] |
BREITBURG D, LEVIN L A, OSCHLIES A, et al.Declining oxygen in the global ocean and coastal waters[J].Science, 2018, 359(6371):eaam7240. doi: 10.1126/science.aam7240
|
[24] |
XIU P, CHAI F, CURCHITSER E N, et al.Future changes in coastal upwelling ecosystems with global warming:the case of the California Current System[J].Scientific Reports, 2018, 8(1):2866. doi: 10.1038/s41598-018-21247-7
|
[25] |
BRISTOW L A, DALSGAARD T, TIANO L, et al.Ammonium and nitrite oxidation at nanomolar oxygen concentrations in oxygen minimum zone waters[J].Proceedings of the National Academy of Sciences of the United States of America, 2016, 113(38):10601-10606. doi: 10.1073/pnas.1600359113
|
[26] |
RAI A K, DAS S S.Late Quaternary changes in surface productivity and oxygen minimum zone (OMZ) in the northwestern Arabian Sea:micropaleontologic and sedimentary record at ODP site 728A[J].Journal of Earth System Science, 2011, 120(1):113-121. doi: 10.1007/s12040-011-0011-7
|
[27] |
CHRONOPOULOU P M, SHELLEY F, PRITCHARD W J, et al.Origin and fate of methane in the Eastern Tropical North Pacific oxygen minimum zone[J].The ISME Journal, 2017, 11(6):1386-1399. doi: 10.1038/ismej.2017.6
|
[28] |
ZHAO H D, KAO S J, ZHAI W D, et al.Effects of stratification, organic matter remineralization and bathymetry on summertime oxygen distribution in the Bohai Sea, China[J].Continental Shelf Research, 2017, 134:15-25. doi: 10.1016/j.csr.2016.12.004
|
[29] |
HELM K P, BINDOFF N L, CHURCH J A.Observed decreases in oxygen content of the global ocean[J].Geophysical Research Letters, 2011, 38(23):L23602. http://www.wanfangdata.com.cn/details/detail.do?_type=perio&id=10.1029/2011GL049513
|
[30] |
LACHKAR Z, LÉVY M, SMITH S.Intensification and deepening of the Arabian Sea oxygen minimum zone in response to increase in Indian monsoon wind intensity[J].Biogeosciences, 2018, 15(1):159-186. doi: 10.5194/bg-15-159-2018
|
[31] |
GERLACH S A.Oxygen conditions improve when the salinity in the Baltic Sea decreases[J].Marine Pollution Bulletin, 1994, 28(7):413-416. doi: 10.1016/0025-326X(94)90126-0
|
[32] |
DAS M, SINGH R K, GUPTA A K, et al.Holocene strengthening of the Oxygen Minimum Zone in the northwestern Arabian Sea linked to changes in intermediate water circulation or Indian monsoon intensity?[J].Palaeogeography, Palaeoclimatology, Palaeoecology, 2017, 483:125-135. doi: 10.1016/j.palaeo.2016.10.035
|
[33] |
XU H B, TANG D L, SHENG J Y, et al.Study of dissolved oxygen responses to tropical cyclones in the Bay of Bengal based on Argo and satellite observations[J].Science of the Total Environment, 2019, 659:912-922. doi: 10.1016/j.scitotenv.2018.12.384
|
[34] |
PINTI D L.Oxygen-minimum zone[M]//GARGAUD M.Encyclopedia of Astrobiology.2nd ed.Berlin, Heidelberg: Springer, 2015: 1-2.
|
[35] |
GIBSON R N, BARNES M, ATKINSON R J A.Temporal and spatial large-scale effects of eutrophication and oxygen deficiency on benthic fauna in Scandinavian and Baltic waters-a review[J].Oceanography and Marine Biology:An Annual Review, 2002, 40:427-489.
|
[36] |
CONLEY D J, BJÖRCK S, BONSDORFF E, et al.Hypoxia-related processes in the Baltic Sea[J].Environmental Science & Technology, 2009, 43(10):3412-3420. http://www.wanfangdata.com.cn/details/detail.do?_type=perio&id=5d7e89936d3667c0791476c2a34778c5
|
[37] |
BERTAGNOLLI A D, STEWART F J.Microbial niches in marine oxygen minimum zones[J].Nature Reviews Microbiology, 2018, 16(12):723-729. doi: 10.1038/s41579-018-0087-z
|
[38] |
LAURENT A, FENNEL K, CAI W J, et al.Eutrophication-induced acidification of coastal waters in the northern Gulf of Mexico:Insights into origin and processes from a coupled physical-biogeochemical model[J].Geophysical Research Letters, 2017, 44(2):946-956. doi: 10.1002/2016GL071881
|
[39] |
GLAZIER A E, ETTER R J.Genetic divergence across an oxygen minimum zone[J].Marine Ecology Progress Series, 2017, 577:79-91. doi: 10.3354/meps12239
|
[40] |
CANFIELD D, THAMDRUP B, KRISTENSEN E.Aquatic geomicrobiology[M].Amsterdam:Academic Press, 2005.
|
[41] |
CALLBECK C M, LAVIK G, FERDELMAN T G, et al.Oxygen minimum zone cryptic sulfur cycling sustained by offshore transport of key sulfur oxidizing bacteria[J].Nature Communications, 2018, 9(1):1729. doi: 10.1038/s41467-018-04041-x
|
[42] |
SAUNDERS J K, FUCHSMAN C A, MCKAY C, et al.Complete arsenic-based respiratory cycle in the marine microbial communities of pelagic oxygen-deficient zones[J].Proceedings of the National Academy of Sciences of the United States of America, 2019, 116(20):9925-9930. doi: 10.1073/pnas.1818349116
|
[43] |
TAVORMINA P L, USSLER III W, STEELE J A, et al.Abundance and distribution of diverse membrane-bound monooxygenase (Cu-MMO) genes within the Costa Rica oxygen minimum zone[J].Environmental Microbiology Reports, 2013, 5(3):414-423. doi: 10.1111/1758-2229.12025
|
[44] |
PADILLA C C, BERTAGNOLLI A D, BRISTOW L A, et al.Metagenomic binning recovers a transcriptionally active gammaproteobacterium linking methanotrophy to partial denitrification in an anoxic oxygen minimum zone[J].Frontiers in Marine Science, 2017, 4:23.
|
[45] |
FRANZ J, KRAHMANN G, LAVIK G, et al.Dynamics and stoichiometry of nutrients and phytoplankton in waters influenced by the oxygen minimum zone in the eastern tropical Pacific[J].Deep Sea Research Part Ⅰ:Oceanographic Research Papers, 2012, 62:20-31. doi: 10.1016/j.dsr.2011.12.004
|
[46] |
GOERICKE R, OLSON R J, SHALAPYONOK A.A novel niche for Prochlorococcus sp.in low-light suboxic environments in the Arabian Sea and the Eastern Tropical North Pacific[J].Deep Sea Research Part Ⅰ:Oceanographic Research Papers, 2000, 47(7):1183-1205. doi: 10.1016/S0967-0637(99)00108-9
|
[47] |
FERNANDES S, MAZUMDAR A, BHATTACHARYA S, et al.Enhanced carbon-sulfur cycling in the sediments of Arabian Sea oxygen minimum zone center[J].Scientific Reports, 2018, 8(1):8665. doi: 10.1038/s41598-018-27002-2
|
[48] |
LÜCKER S, NOWKA B, RATTEI T, et al.The genome of Nitrospina gracilis illuminates the metabolism and evolution of the major marine nitrite oxidizer[J].Frontiers in Microbiology, 2013, 4:27. http://d.old.wanfangdata.com.cn/OAPaper/oai_pubmedcentral.nih.gov_3578206
|
[49] |
PREISIG O, ZUFFEREY R, THÖNY-MEYER L, et al.A high-affinity cbb3-type cytochrome oxidase terminates the symbiosis-specific respiratory chain of Bradyrhizobium japonicum[J].Journal of Bacteriology, 1996, 178(6):1532-1528. doi: 10.1128/JB.178.6.1532-1538.1996
|
[50] |
REVSBECH N P, HAUER LARSEN L, GUNDERSEN J, et al.Determination of ultra-low oxygen concentrations in oxygen minimum zones by the STOX sensor[J].Limnology and Oceanography, Methods, 2009, 7(5):371-381. doi: 10.4319/lom.2009.7.371
|
[51] |
PENG X F, FUCHSMAN C A, JAYAKUMAR A, et al.Revisiting nitrification in the Eastern Tropical South Pacific:a focus on controls[J].Journal of Geophysical Research, 2016, 121(3):1667-1684. http://smartsearch.nstl.gov.cn/paper_detail.html?id=86f4cea8492aee9948d32b3acf0106a8
|
[52] |
BRANDHORST W.Nitrification and denitrification in the eastern Tropical North Pacific[J].ICES Journal of Marine Science, 1959, 25(1):3-20. doi: 10.1093/icesjms/25.1.3
|
[53] |
LAM P, LAVIK G, JENSEN M M, et al.Revising the nitrogen cycle in the Peruvian oxygen minimum zone[J].Proceedings of the National Academy of Sciences of the United States of America, 2009, 106(12):4752-4757. doi: 10.1073/pnas.0812444106
|
[54] |
FRANCIS C A, ROBERTS K J, BEMAN J M, et al.Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean[J].Proceedings of the National Academy of Sciences of the United States of America, 2005, 102(41):14683-14688. doi: 10.1073/pnas.0506625102
|
[55] |
BRYANT J A, STEWART F J, EPPLEY J M, et al.Microbial community phylogenetic and trait diversity declines with depth in a marine oxygen minimum zone[J].Ecology, 2012, 93(7):1659-1673. doi: 10.1890/11-1204.1
|
[56] |
MILLER D R, PFREUNDT U, ELIFANTZ H, et al.Microbial metatranscriptomes from the thermally stratified Gulf of Aqaba/Eilat during summer[J].Marine Genomics, 2017, 32:23-26. doi: 10.1016/j.margen.2016.12.001
|
[57] |
STEVENS H, ULLOA O.Bacterial diversity in the oxygen minimum zone of the eastern tropical South Pacific[J].Environmental Microbiology, 2008, 10(5):1244-1259. doi: 10.1111/j.1462-2920.2007.01539.x
|
[58] |
MA Y, ZENG Y H, JIAO N Z, et al.Vertical distribution and phylogenetic composition of bacteria in the Eastern Tropical North Pacific Ocean[J].Microbiological Research, 2009, 164(6):624-633. doi: 10.1016/j.micres.2008.01.001
|
[59] |
PODLASKA A, WAKEHAM S G, FANNING K A, et al.Microbial community structure and productivity in the oxygen minimum zone of the eastern tropical North Pacific[J].Deep Sea Research Part Ⅰ:Oceanographic Research Papers, 2012, 66:77-89. doi: 10.1016/j.dsr.2012.04.002
|
[60] |
GONSALVES M J, PAROPKARI A L, FERNANDES C E G, et al.Predominance of anaerobic bacterial community over aerobic community contribute to intensify 'oxygen minimum zone' in the eastern Arabian Sea[J].Continental Shelf Research, 2011, 31(11):1224-1235. doi: 10.1016/j.csr.2011.04.011
|
[61] |
NOBU M K, NARIHIRO T, RINKE C, et al.Microbial dark matter ecogenomics reveals complex synergistic networks in a methanogenic bioreactor[J].The ISME Journal, 2015, 9(8):1710-1722. doi: 10.1038/ismej.2014.256
|
[62] |
SCHNETZER A, MOORTHI S D, COUNTWAY P D, et al.Depth matters:microbial eukaryote diversity and community structure in the eastern North Pacific revealed through environmental gene libraries[J].Deep Sea Research Part Ⅰ:Oceanographic Research Papers, 2011, 58(1):16-26. doi: 10.1016/j.dsr.2010.10.003
|
[63] |
JING H, ROCKE E, KONG L, et al.Protist communities in a marine oxygen minimum zone off Costa Rica by 454 pyrosequencing[J].Biogeosciences Discussions, 2015, 12(16):13483-13509. doi: 10.5194/bgd-12-13483-2015
|
[64] |
STEWART F J, ULLOA O, DELONG E F.Microbial metatranscriptomics in a permanent marine oxygen minimum zone[J].Environmental Microbiology, 2012, 14(1):23-40. doi: 10.1111/j.1462-2920.2010.02400.x
|
[65] |
BRISTOW L A, SARODE N, CARTEE J, et al.Biogeochemical and metagenomic analysis of nitrite accumulation in the Gulf of Mexico hypoxic zone[J].Limnology and Oceanography, 2015, 60(5):1733-1750. doi: 10.1002/lno.10130
|
[66] |
MONTEIRO M, SÉNECA J, MAGALHÃES C.The history of aerobic ammonia oxidizers:from the first discoveries to today[J].Journal of Microbiology, 2014, 52(7):537-547. doi: 10.1007/s12275-014-4114-0
|
[67] |
WANG S Y, RADNY D, HUANG S B, et al.Nitrogen loss by anaerobic ammonium oxidation in unconfined aquifer soils[J].Scientific Reports, 2017, 7(1):40173. doi: 10.1038/srep40173
|
[68] |
SCHMID M C, RISGAARD-PETERSEN N, VAN DE VOSSENBERG J, et al.Anaerobic ammonium-oxidizing bacteria in marine environments:widespread occurrence but low diversity[J].Environmental Microbiology, 2007, 9(6):1476-1484. doi: 10.1111/j.1462-2920.2007.01266.x
|
[69] |
DALSGAARD T, THAMDRUP B, FARÍAS L, et al.Anammox and denitrification in the oxygen minimum zone of the eastern South Pacific[J].Limnology and Oceanography, 2012, 57(5):1331-1346. doi: 10.4319/lo.2012.57.5.1331
|
[70] |
CASCIOTTI K L, BUCHWALD C.Insights on the marine microbial nitrogen cycle from isotopic approaches to nitrification[J].Frontiers in Microbiology, 2012, 3:356. http://d.old.wanfangdata.com.cn/OAPaper/oai_pubmedcentral.nih.gov_3469838
|
[71] |
GLASS J B, KRETZ C B, GANESH S, et al.Meta-omic signatures of microbial metal and nitrogen cycling in marine oxygen minimum zones[J].Frontiers in Microbiology, 2015, 6:998. http://www.wanfangdata.com.cn/details/detail.do?_type=perio&id=Doaj000004600265
|
[72] |
HAWLEY A K, BREWER H M, NORBECK A D, et al.Metaproteomics reveals differential modes of metabolic coupling among ubiquitous oxygen minimum zone microbes[J].Proceedings of the National Academy of Sciences of the United States of America, 2014, 111(31):11395-11400. doi: 10.1073/pnas.1322132111
|