Pacific oyster (Crassostrea gigas) stocking density as a regulator of nitrous oxide emissions: connecting sediment biogeochemistry and microbial functional genes

Shengjie Xu , Li Li , Xuan Dong , Miaojun Pan , Wenwen Jiang , Xiangli Tian , Yunwei Dong , Shuanglin Dong , Ramón Filgueira

Marine Life Science & Technology ›› : 1 -13.

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Marine Life Science & Technology ›› :1 -13. DOI: 10.1007/s42995-026-00387-0
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Pacific oyster (Crassostrea gigas) stocking density as a regulator of nitrous oxide emissions: connecting sediment biogeochemistry and microbial functional genes
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Abstract

Bivalves play a key role in regulating the biogeochemistry of coastal systems, particularly by enhancing nitrogen recycling in sediments. However, the impact of these processes on sediment nitrous oxide (N2O) emissions—a potent greenhouse gas—remains poorly understood, limiting our ability to develop effective mitigation strategies. This study investigated N2O fluxes at the sediment–water interface in a 120 day land-based enclosure experiment with Pacific oysters (Crassostrea gigas) at four stocking densities and a control group. The results showed that sediments consistently acted as N2O sources, with the highest stocking density exhibiting significantly greater N2O fluxes due to increased particulate organic carbon (POC) and nitrogen (PON) deposition. Oyster aquaculture significantly altered sediment biogeochemistry, and random forest modeling identified pore water nitrate as a strong predictor of N2O flux. The nirK gene abundance increased while nosZ gene abundance decreased in the highest stocking density group, resulting in an elevated nir/nosZ ratio. Structural equation modeling further indicated that oyster density indirectly increased N2O flux by altering pore water physicochemical properties. Although local environmental conditions modulate N2O fluxes, this study elucidates how stocking density drives N2O emissions via biogeochemistry and microbial pathways, highlighting that managing stocking density is a key consideration for mitigating the climate footprint of aquaculture.

Keywords

N2O fluxes / Oyster / Sediment–water interface / N-cycling genes

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Shengjie Xu, Li Li, Xuan Dong, Miaojun Pan, Wenwen Jiang, Xiangli Tian, Yunwei Dong, Shuanglin Dong, Ramón Filgueira. Pacific oyster (Crassostrea gigas) stocking density as a regulator of nitrous oxide emissions: connecting sediment biogeochemistry and microbial functional genes. Marine Life Science & Technology 1-13 DOI:10.1007/s42995-026-00387-0

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References

[1]

Al MA, Wang YF, Huang J, Yu YH, Juneau P, He ZL, Yan QY. Anammox and denitrifying bacteria and their nitrogen removal potential in lake sediments mediated by environmental changes. Mar Life Sci Technol, 2025, 7: 670-681

[2]

Berner RAEarly diagenesis: A theoretical approach, 1980PrincetonPrinceton University Press

[3]

Bureau of Fisheries, Ministry of Agriculture and Rural Affairs of the People’s Republic of ChinaChina Fishery Statistical Yearbook, 2025, 2025BeijingChina Agriculture Press

[4]

Chen HB, Zeng L, Wang DB, Zhou YY, Yang X. Recent advances in nitrous oxide production and mitigation in wastewater treatment. Water Res, 2020, 184 Article ID: 116168

[5]

Chen GZ, Bai JH, Bi C, Wang YQ, Cui BS. Global greenhouse gas emissions from aquaculture: a bibliometric analysis. Agric Ecosyst Environ, 2023, 348 Article ID: 108405

[6]

Chen XWJ, Zhang Z, Pan MJ, Liu Y, Li CL, Zhou YG, Li L, Dong X, Dong YW, Li JY, Liu SM, Wang XN, Tian SJ, Liu Y, Zhang JH, Qiu YG, Wang XG, Cai WJ, Tian XL, Kao SJ, Dong SL. Oyster farming acts as a marine carbon dioxide removal (mCDR) hotspot for climate change mitigation. PNAS, 2025, 122 Article ID: e2504004122

[7]

Crossland NO, Lapoint TW. The design of mesocosm experiments. Environ Toxicol Chem, 1992, 11: 1-4

[8]

Daly EJ, Hernandez-Ramirez G, Congreves KA, Clough T, Voigt C, Harris E, Ruser R. Soil organic nitrogen priming to nitrous oxide: a synthesis. Soil Biol Biochem, 2024, 189 Article ID: 109254

[9]

Deng ML, Zheng Y, He ZY, Lyu M, Jin SS, Yang H, Zhang HS, He JZ, Lin YX. Organic carbon negatively affects the diversity of soil nitrous oxide reducers in Chinese fir plantations at a regional scale. Appl Soil Ecol, 2024, 200 Article ID: 105457

[10]

Dong YH, Yuan JJ, Li JJ, Liu DY, Wu X, Zheng HJ, Wang H, Wang HQ, Ding WX. Divergent impacts of animal bioturbation on methane and nitrous oxide emissions from mariculture ponds. Water Res, 2025, 270 Article ID: 122822

[11]

Donis D, Flury S, Stöckli A, Spangenberg JE, Vachon D, McGinnis DF. Full-scale evaluation of methane production under oxic conditions in a mesotrophic lake. Nat Commun, 2017, 8 Article ID: 1661

[12]

Erler DV, Welsh DT, Bennet WW, Meziane T, Hubas C, Nizzoli D, Ferguson AJP. The impact of suspended oyster farming on nitrogen cycling and nitrous oxide production in a sub-tropical Australian estuary. Estuar Coast Shelf Sci, 2017, 192: 117-127

[13]

Feng R, Fang X. Devoting attention to China’s burgeoning industrial N2O emissions. Environ Sci Technol, 2022, 56: 5299-5301

[14]

Feng JF, Liu YB, Li FB, Zhou XY, Xu CC, Fang FP. Effect of phosphorus and potassium addition on greenhouse gas emissions and nutrient utilization of a rice-fish co-culture system. Environ Sci Pollut Res, 2021, 28: 38034-38042

[15]

Filgueira R, Byron CJ, Comeau LA, Costa-Pierce B, Cranford PJ, Ferreira JG, Grant J, Guyondet T, Jansen HM, Landry T. An integrated ecosystem approach for assessing the potential role of cultivated bivalve shells as part of the carbon trading system. Mar Ecol Prog Ser, 2015, 518: 281-287

[16]

Gornshteyn BJ. Fick’s first law of diffusion and binary gas separation by hollow-fiber asymmetric membrane. Can J Chem Eng, 2008, 81: 139-146

[17]

Hama-Aziz ZQ, Hiscock KM, Cooper RJ. Indirect nitrous oxide emission factors for agricultural field drains and headwater streams. Environ Sci Technol, 2017, 51: 301-307

[18]

Hu Z, Lee JW, Chandran K, Kim S, Khanal SK. Nitrous oxide (N2O) emission from aquaculture: a review. Environ Sci Technol, 2012, 46: 6470-6480

[19]

Hutchins DA, Capone DG. The marine nitrogen cycle: new developments and global change. Nat Rev Microbiol, 2022, 20: 401-414

[20]

Jansson JK, Hofmockel KS. The soil microbiome—from metagenomics to metaphenomics. Curr Opin Microbiol, 2018, 43: 162-168

[21]

Ji QX, Babbin AR, Peng XF, Bowen JL, Ward BB. Nitrogen substrate-dependent nitrous oxide cycling in salt marsh sediments. J Mar Res, 2015, 73: 71-92

[22]

Jiang ZB, Du P, Liao YB, Liu Q, Chen QZ, Shou L, Zeng JN, Chen JF. Oyster farming control on phytoplankton bloom promoted by thermal discharge from a power plant in a eutrophic, semi-enclosed bay. Water Res, 2019, 159: 1-9

[23]

Larionov A, Krause A, Miller W. A standard curve based method for relative real time PCR data processing. BMC Bioinformatics, 2005, 6: 62

[24]

Lavery PS, Oldham CE, Ghisalberti M. The use of Fick’s First Law for predicting porewater nutrient fluxes under diffusive conditions. Hydrol Process, 2001, 15: 2435-2451

[25]

Liu RR, Tian Y, Zhou EM, Xiong MJ, Xiao M, Li WJ. Distinct expression of the two NO-forming nitrite reductases in Thermus antranikianii DSM 12462T improved environmental adaptability. Microb Ecol, 2020, 80: 614-626

[26]

Lycus P, Soriano-Laguna MJ, Kjos M, Richardson DJ, Gates AJ, Milligan DA, Frostegård Å, Bergaust L, Bakken LR. A bet-hedging strategy for denitrifying bacteria curtails their release of N2O. Proc Natl Acad Sci U S A, 2018, 115: 11820-11825

[27]

Mao CZ, Li XH, Dunthorn M, Xu WX, Luo XT, Xiong XP, Al-Farraj SA, Huang J. Diversity and assembly mechanisms of zooplankton communities in freshwater aquaculture ponds. Mar Life Sci Technol, 2025, 7: 549-564

[28]

Ming YZ, Abdullah AM, Zhang DD, Zhu WG, Liu HP, Cai LL, Yu XL, Wu K, Niu MY, Zeng QL. Insights into the evolutionary and ecological adaption strategies of nirS- and nirK-type denitrifying communities. Mol Ecol, 2024, 33 Article ID: e17507

[29]

Moran MA, Satinsky B, Gifford SM, Luo HW, Rivers A, Chan LK, Meng J, Durham BP, Shen C, Varaljay VA, Smith CB, Yager PL, Hopkinson BM. Sizing up metatranscriptomics. ISME J, 2013, 7: 237-243

[30]

Naylor RL, Kishore A, Sumaila UR, Issifu I, Hunter BP, Belton B, Bush SR, Cao L, Gelcich S, Gephart JA. Blue food demand across geographic and temporal scales. Nat Commun, 2021, 12: 5799

[31]

Newell RIE. Ecosystem influences of natural and cultivated populations of suspension-feeding bivalve molluscs: a review. J Shellfish Res, 2004, 23: 51-61

[32]

Porter ET, Cornwell JC, Sanford LP. Effect of oysters Crassostrea virginica and bottom shear velocity on benthic-pelagic coupling and estuarine water quality. Mar Ecol Prog Ser, 2004, 271: 61-75

[33]

Ray NE, Fulweiler RW. Negligible greenhouse gas release from sediments in oyster habitats. Environ Sci Technol, 2021, 55: 14225-14233

[34]

Ray NE, Fulweiler RW. Meta-analysis of oyster impacts on coastal biogeochemistry. Nat Sustain, 2021, 4: 261-269

[35]

Ray NE, Maguire TJ, Al-Haj AN, Henning MC, Fulweiler RW. Low greenhouse gas emissions from oyster aquaculture. Environ Sci Technol, 2019, 53: 9118-9127

[36]

Rice EW, Bridgewater LAmerican Public Health AssociationStandard methods for the examination of water and wastewater, 2012WashingtonAmerican Public Health Association

[37]

Smyth AR, Geraldi NR, Piehler MF. Oyster-mediated benthic-pelagic coupling modifies nitrogen pools and processes. Mar Ecol Prog Ser, 2013, 493: 23-30

[38]

Smyth AR, Geraldi NR, Thompson SP, Piehler MF. Biological activity exceeds biogenic structure in influencing sediment nitrogen cycling in experimental oyster reefs. Mar Ecol Prog Ser, 2016, 560: 173-183

[39]

Smyth AR, Murphy AE, Anderson IC, Song B. Differential effects of bivalves on sediment nitrogen cycling in a shallow coastal bay. Estuar Coast, 2018, 41: 1147-1163

[40]

Song WM, Zhao Y, Zhou J, Feng JX, Wang ZL, Han GX, Pendall E, Lin GH. The effects of climate warming and exogenous nitrogen input on soil N2O emissions from mangroves. Soil Biol Biochem, 2024, 199 Article ID: 109607

[41]

Stewart RIA, Dossena M, Bohan DA, Jeppesen E, Kordas RL, Ledger ME, Meerhoff M, Moss B, Mulder C, Shurin JB. Mesocosm experiments as a tool for ecological climate-change research. Adv Ecol Res, 2013, 48: 71-181

[42]

Sun H, Yu R, Liu X, Cao Z, Li X, Zhang Z, Wang J, Zhuang S, Ge Z, Zhang L, Sun L, Lorke A, Yang J, Lu C, Lu X. Drivers of spatial and seasonal variations of CO2 and CH4 fluxes at the sediment water interface in a shallow eutrophic lake. Water Res, 2022, 222 Article ID: 118916

[43]

Tamimi A, Rinker EB, Sandall OC. Diffusion coefficients for hydrogen sulfide, carbon dioxide, and nitrous oxide in water over the temperature range 293–368 K. J Chem Eng Data, 1994, 39: 330-332

[44]

Tian Y, Yang P, Yang H, Wang H, Zhang L, Tong C, Lai DYF, Lin Y, Tan L, Hong Y, Tang C, Tang KW. Diffusive nitrous oxide (N2O) fluxes across the sediment-water-atmosphere interfaces in aquaculture shrimp ponds in a subtropical estuary: implications for climate warming. Agric Ecosyst Environ, 2023, 341 Article ID: 108218

[45]

Welsh DT, Nizzoli D, Fano EA, Viaroli P. Direct contribution of clams (Ruditapes philippinarum) to benthic fluxes, nitrification, denitrification and nitrous oxide emission in a farmed sediment. Estuar Coast Shelf Sci, 2015, 154: 84-93

[46]

Yang P, Wang DQ, Lai DYF, Zhang YF, Guo QQ, Tan LS, Yang H, Tong C, Li XF. Spatial variations of N2O fluxes across the water-air interface of mariculture ponds in a subtropical estuary in Southeast China. J Geophys Res Biogeosci, 2020, 125 Article ID: e2019JG005605

[47]

Yang P, Tang KW, Tong C, Lai DYF, Zhang LH, Lin X, Yang H, Tan LS, Zhang YF, Hong Y, Tang C, Lin YX. Conversion of coastal wetland to aquaculture ponds decreased N2O emission: evidence from a multi-year field study. Water Res, 2022, 227 Article ID: 119326

[48]

Yuan JJ, Liu DY, Xiang J, He TH, Kang H, Ding WX. Methane and nitrous oxide have separated production zones and distinct emission pathways in freshwater aquaculture ponds. Water Res, 2021, 190 Article ID: 116739

[49]

Zhang W, Li H, Xiao Q, Li X. Urban rivers are hotspots of riverine greenhouse gas (N2O, CH4, CO2) emissions in the mixed-landscape Chaohu lake basin. Water Res, 2021, 189 Article ID: 116624

[50]

Zhang Y, Chen MM, Du R, Tan E, Kao S-J, Zhang Y. Critical roles of rare species in the anaerobic ammonium oxidizing bacterial community in coastal sediments. Mar Life Sci Technol, 2025, 7: 507-522

[51]

Zhang H, Cheong KL, Tan KR. Bivalves as climate-friendly high quality animal protein: a comprehensive review. Food Secur, 2025, 17: 739-748

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