Microbial Ecology under Ocean Deoxygenation: Diversity, Metabolisms, Environmental Controls

Peihang Xu

doi:10.21996/nag8-j503

Microbial Ecology under Ocean Deoxygenation: Diversity, Metabolisms, Environmental Controls

Peihang Xu^*

^*Kontaktforfatter

Publikation: Afhandling › Ph.d.-afhandling

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Abstract

Iltminimumszoner (OMZ'er) i verdenshavene skabes og opretholdes af den komplekse interaktion mellem forbrug og produktion i biologiske processer samt fysiske forsyningsmekanismer. Desoxidation og fortsat udvidelse af OMZ'er peger på en voksende betydningsfuld rolle for OMZmikrober i globale biogeokemiske cyklusser. Dog mangler der i øjeblikket en omfattende analyse og sammenligning af de væsentligste biologiske cyklusser udført af mikrobielle samfund inden for marine OMZ'er og ikke-OMZ-miljøer over langvarige tidsperioder eller brede regionale skalaer. Denne afhandling undersøgte mikrobiel mangfoldighed, fordeling og deres vigtigste metabolismer under havets desoxidation med forskellige fokusområder i tre store oceaniske iltminimumszoner (OMZs): Det tropiske sydatlantiske område (TSA, Manuskript Ⅰ), det østlige tropiske Stillehav (ETP, Manuskript Ⅱ) og Østersøen (Manuskript Ⅲ). Manuskript Ⅰ afslørede en negativ sammenhæng mellem ilt/nitritniveauer og udbredelsen af de fleste kvælstofveje (f.eks. nitratreduktion og nitritoxidation, nitrifikation og denitrifikation (N2O-produktion)), kulstofveje (f.eks. CO-oxidation og methanogenese), phosphorveje (f.eks. alkalisk fosfatase) og svovlveje (f.eks. sulfidoxidation). Disse veje viste tendens til at have højere forekomst, når OMZ'er udvider sig, og opstrømning bliver hyppigere eller stærkere i TSA. Visse dominerende faktorer (f.eks. SAR11, Nitrospina, Thermoproteota) og deres genetiske potentiale blev fremhævet. Både den relative forekomst af veje for N2O-forbrug og produktion viste positive sammenhænge med N2O-indholdet. Manuskript Ⅱ involverede tidsmæssig skala for at undersøge OMZ-udvidelse og ENSO-hændelsernes indvirkning på mikrobiel mangfoldighed og metabolismer i ETP. På trods af forekomsten af flere ENSOhændelser fra 2011-2022, herunder en kraftig El Niño i 2015-2016, forekom der minimale variationer i mikrobiel mangfoldighed eller taksonomi i ETP. Dog observerede vi en betydelig reduktion i den relative rigdom af SAR11, ledsaget af en stigning i potentialet for kvælstofmetabolismer som f.eks. denitrifikation (N2O-produktion) og kvælstoffiksering, både i den fotiske zone og kernen af OMZ'en. Derudover aftager den mikrobielle mængde og nogle metabolismer (f.eks. fosfattransport og regulering, kvælstoffiksering), men flertallet af kvælstofmetabolismerne øges langs iltningsgradienten fra oksisk til suboksisk. Forskellige dominante mikrobielle grupper, der agerer i vitale biogeokemiske cyklusser, udviste forskellige følsomheder over for iltniveauer, og bemærkelsesværdige skift i adskillige funktionelle grupper blev observeret ved iltningstærskler på 120, 90, 80, 60 og 12 µmol/kg. Desuden var den relative forekomst af Thermoproteota, der koder for nitritreduktase (nirK), positivt korreleret med N2O-indholdet, men negativt korreleret med iltniveauet, hvilket antyder en stigning i N2O produceret af Thermoproteota under OMZ-udvidelse. Manuskript Ⅲ undersøgte den rumlige fordeling og aktivitet af anaerobe (AP) og aerobe fototrofer (OP) i Østersøen. Der blev afsløret en rig mangfoldighed af OP og AP. OP udviste aktiv fotosyntese, mens AP ikke viste nogen påviselig fotosyntese i de fleste stationer. Både cyanobakterielle og eukaryote OP foretrak højere temperaturer og øvre vandlag. AP viste ikke en markant hydro kemisk præference, men tendens til at eksistere sammen med OP-samfundet. Som helhed giver denne afhandling indsigt i, hvordan mikrobiel mangfoldighed, forskellige grupper og funktioner vil reagere på klimaændringsinduceret udvidelse af OMZ i et bredt marineperspektiv.

Originalsprog	Engelsk
Bevilgende institution	Syddansk Universitet
Vejledere/rådgivere	Löscher, Carolin, Hovedvejleder
Dato for forsvar	8. sep. 2023
Udgiver	Syddansk Universitet. Det Naturvidenskabelige Fakultet
DOI	https://doi.org/10.21996/nag8-j503
Status	Udgivet - 28. aug. 2023

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10.21996/nag8-j503

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1 Tidsskriftartikel

Spatial Distribution, Diversity, and Activity of Microbial Phototrophs in the Baltic Sea
Xu, P., Reeder, C. F. & Löscher, C. R., jan. 2022, I: Frontiers in Marine Science. 8, 19 s., 773210.
Publikation: Bidrag til tidsskrift › Tidsskriftartikel › Forskning › peer review

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Anoxygenic phototrophs in Oxygen Minimum Zones
Xu, P. (Projektdeltager)
01/10/2019 → 30/09/2022
Projekter: Projekt › Ph.d-projekt

Citationsformater

@misc{b19b6e0dafc34fe4abe78a021458c39d,

title = "Microbial Ecology under Ocean Deoxygenation: Diversity, Metabolisms, Environmental Controls",

abstract = "Oxygen minimum zones (OMZs) in the global oceans are formed and sustained by the complex interaction between biological processes of consumption and production, as well as physical supply mechanisms. Deoxygenation and continuous OMZ expansion point to a growing significant role of OMZ microbes in global biogeochemical cycles. However, comprehensive analysis and comparison of key cycles performed by microbial communities within marine OMZs and non-OMZ environments over large timescales or broad regional scales are currently lacking.This thesis studied the microbial diversity, distribution, and their key metabolisms under ocean deoxygenation with different focuses in three large oceanic OMZs: the Tropical South Atlantic (TSA, Manuscript Ⅰ), the Eastern Tropical Pacific (ETP, Manuscript Ⅱ), and the Baltic Sea (Manuscript Ⅲ). Manuscript Ⅰ revealed a negative correlation between oxygen/nitrite levels and the prevalence of most nitrogen pathways (e.g., nitrate reduction and nitrite oxidation, nitrification, and denitrification (N2O production)), carbon pathways (e.g., CO oxidation and methanogenesis), phosphorus pathways (e.g., alkaline phosphatase), and sulfur pathways (e.g., sulfide oxidation). These pathways tended to exhibit higher abundances when the OMZs expand and upwelling turns more frequent or stronger in the TSA. Certain predominant drivers (e.g., SAR11, Nitrospina, Thermoproteota) and their genetic potentials were emphasized. Both the relative abundance of pathways of N2O consumption and production showed positive correlations with N2O content. Manuscript Ⅱ involved the temporal scale for studying the OMZ expansion and ENSO events on microbial diversity and metabolisms in the ETP. Despite the occurrence of multiple ENSO events from 2011-2022, including a strong El Ni{\~n}o in 2015- 2016, there appeared to be minimal variations in microbial diversity or taxonomy in the ETP. However, we did observe a significant decrease in the relative abundance of SAR11, accompanied by an increase in the potential for nitrogen metabolisms, such as denitrification (N2O production) and nitrogen fixation, both in the euphotic layer and the core of the OMZ. Moreover, the microbial abundance and some metabolisms (e.g., phosphate transport and regulation, nitrogen fixation) decreases but majority of nitrogen metabolisms increase along the oxygen gradient from oxic to suboxic. Distinct microbial dominant groups participating in essential biogeochemical cycles exhibited varying sensitivities to oxygen levels, and noticeable shifts in numerous functional groups were observed at oxygen thresholds of 120, 90, 80, 60, and 12 µmol/kg. Furthermore, the relative abundance of Thermoproteota encoding nitrite reductase (nirK) was positively correlated with N2O content but negatively correlated with oxygen, suggesting an increase of the N2O produced by Thermoproteota under OMZ expansion. Manuscript Ⅲ studied the spatial distribution and activity of anoxygenic (AP) and oxygenic phototrophs (OP) in the Baltic Sea. A rich diversity of OP and AP was revealed. OP exhibited active photosynthesis, while AP showed no detectable photosynthesis in most stations. Both cyanobacterial and eukaryotic OP preferred higher temperatures and upper water layers. AP did not show a significant hydrochemical preference but tended to coexist with the OP community. Overall, this thesis provide insights of how microbial diversity, diverse groups and functions would respond towards climate change induced OMZ expansion in a broad marine scope.",

author = "Peihang Xu",

year = "2023",

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doi = "10.21996/nag8-j503",

language = "English",

publisher = "Syddansk Universitet. Det Naturvidenskabelige Fakultet",

address = "Denmark",

school = "SDU",

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T1 - Microbial Ecology under Ocean Deoxygenation: Diversity, Metabolisms, Environmental Controls

AU - Xu, Peihang

PY - 2023/8/28

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N2 - Oxygen minimum zones (OMZs) in the global oceans are formed and sustained by the complex interaction between biological processes of consumption and production, as well as physical supply mechanisms. Deoxygenation and continuous OMZ expansion point to a growing significant role of OMZ microbes in global biogeochemical cycles. However, comprehensive analysis and comparison of key cycles performed by microbial communities within marine OMZs and non-OMZ environments over large timescales or broad regional scales are currently lacking.This thesis studied the microbial diversity, distribution, and their key metabolisms under ocean deoxygenation with different focuses in three large oceanic OMZs: the Tropical South Atlantic (TSA, Manuscript Ⅰ), the Eastern Tropical Pacific (ETP, Manuscript Ⅱ), and the Baltic Sea (Manuscript Ⅲ). Manuscript Ⅰ revealed a negative correlation between oxygen/nitrite levels and the prevalence of most nitrogen pathways (e.g., nitrate reduction and nitrite oxidation, nitrification, and denitrification (N2O production)), carbon pathways (e.g., CO oxidation and methanogenesis), phosphorus pathways (e.g., alkaline phosphatase), and sulfur pathways (e.g., sulfide oxidation). These pathways tended to exhibit higher abundances when the OMZs expand and upwelling turns more frequent or stronger in the TSA. Certain predominant drivers (e.g., SAR11, Nitrospina, Thermoproteota) and their genetic potentials were emphasized. Both the relative abundance of pathways of N2O consumption and production showed positive correlations with N2O content. Manuscript Ⅱ involved the temporal scale for studying the OMZ expansion and ENSO events on microbial diversity and metabolisms in the ETP. Despite the occurrence of multiple ENSO events from 2011-2022, including a strong El Niño in 2015- 2016, there appeared to be minimal variations in microbial diversity or taxonomy in the ETP. However, we did observe a significant decrease in the relative abundance of SAR11, accompanied by an increase in the potential for nitrogen metabolisms, such as denitrification (N2O production) and nitrogen fixation, both in the euphotic layer and the core of the OMZ. Moreover, the microbial abundance and some metabolisms (e.g., phosphate transport and regulation, nitrogen fixation) decreases but majority of nitrogen metabolisms increase along the oxygen gradient from oxic to suboxic. Distinct microbial dominant groups participating in essential biogeochemical cycles exhibited varying sensitivities to oxygen levels, and noticeable shifts in numerous functional groups were observed at oxygen thresholds of 120, 90, 80, 60, and 12 µmol/kg. Furthermore, the relative abundance of Thermoproteota encoding nitrite reductase (nirK) was positively correlated with N2O content but negatively correlated with oxygen, suggesting an increase of the N2O produced by Thermoproteota under OMZ expansion. Manuscript Ⅲ studied the spatial distribution and activity of anoxygenic (AP) and oxygenic phototrophs (OP) in the Baltic Sea. A rich diversity of OP and AP was revealed. OP exhibited active photosynthesis, while AP showed no detectable photosynthesis in most stations. Both cyanobacterial and eukaryotic OP preferred higher temperatures and upper water layers. AP did not show a significant hydrochemical preference but tended to coexist with the OP community. Overall, this thesis provide insights of how microbial diversity, diverse groups and functions would respond towards climate change induced OMZ expansion in a broad marine scope.

AB - Oxygen minimum zones (OMZs) in the global oceans are formed and sustained by the complex interaction between biological processes of consumption and production, as well as physical supply mechanisms. Deoxygenation and continuous OMZ expansion point to a growing significant role of OMZ microbes in global biogeochemical cycles. However, comprehensive analysis and comparison of key cycles performed by microbial communities within marine OMZs and non-OMZ environments over large timescales or broad regional scales are currently lacking.This thesis studied the microbial diversity, distribution, and their key metabolisms under ocean deoxygenation with different focuses in three large oceanic OMZs: the Tropical South Atlantic (TSA, Manuscript Ⅰ), the Eastern Tropical Pacific (ETP, Manuscript Ⅱ), and the Baltic Sea (Manuscript Ⅲ). Manuscript Ⅰ revealed a negative correlation between oxygen/nitrite levels and the prevalence of most nitrogen pathways (e.g., nitrate reduction and nitrite oxidation, nitrification, and denitrification (N2O production)), carbon pathways (e.g., CO oxidation and methanogenesis), phosphorus pathways (e.g., alkaline phosphatase), and sulfur pathways (e.g., sulfide oxidation). These pathways tended to exhibit higher abundances when the OMZs expand and upwelling turns more frequent or stronger in the TSA. Certain predominant drivers (e.g., SAR11, Nitrospina, Thermoproteota) and their genetic potentials were emphasized. Both the relative abundance of pathways of N2O consumption and production showed positive correlations with N2O content. Manuscript Ⅱ involved the temporal scale for studying the OMZ expansion and ENSO events on microbial diversity and metabolisms in the ETP. Despite the occurrence of multiple ENSO events from 2011-2022, including a strong El Niño in 2015- 2016, there appeared to be minimal variations in microbial diversity or taxonomy in the ETP. However, we did observe a significant decrease in the relative abundance of SAR11, accompanied by an increase in the potential for nitrogen metabolisms, such as denitrification (N2O production) and nitrogen fixation, both in the euphotic layer and the core of the OMZ. Moreover, the microbial abundance and some metabolisms (e.g., phosphate transport and regulation, nitrogen fixation) decreases but majority of nitrogen metabolisms increase along the oxygen gradient from oxic to suboxic. Distinct microbial dominant groups participating in essential biogeochemical cycles exhibited varying sensitivities to oxygen levels, and noticeable shifts in numerous functional groups were observed at oxygen thresholds of 120, 90, 80, 60, and 12 µmol/kg. Furthermore, the relative abundance of Thermoproteota encoding nitrite reductase (nirK) was positively correlated with N2O content but negatively correlated with oxygen, suggesting an increase of the N2O produced by Thermoproteota under OMZ expansion. Manuscript Ⅲ studied the spatial distribution and activity of anoxygenic (AP) and oxygenic phototrophs (OP) in the Baltic Sea. A rich diversity of OP and AP was revealed. OP exhibited active photosynthesis, while AP showed no detectable photosynthesis in most stations. Both cyanobacterial and eukaryotic OP preferred higher temperatures and upper water layers. AP did not show a significant hydrochemical preference but tended to coexist with the OP community. Overall, this thesis provide insights of how microbial diversity, diverse groups and functions would respond towards climate change induced OMZ expansion in a broad marine scope.

U2 - 10.21996/nag8-j503

DO - 10.21996/nag8-j503

M3 - Ph.D. thesis

PB - Syddansk Universitet. Det Naturvidenskabelige Fakultet

ER -

Microbial Ecology under Ocean Deoxygenation: Diversity, Metabolisms, Environmental Controls

Abstract

Dokumenter og links

SDU link

Fingeraftryk

Relaterede publikationer

Spatial Distribution, Diversity, and Activity of Microbial Phototrophs in the Baltic Sea

Relaterede projekter

Anoxygenic phototrophs in Oxygen Minimum Zones

Citationsformater