Temperature adaptability of dark carbon fixation in seawater fromthe Yangtze River Estuary

doi:10.3969/j.issn.1000-5641.2024.01.011

Abstract

Abstract:

To clarify the effects of global warming on dark carbon fixation (DCF) in eutrophic estuaries, the rates of total DCF and DCF driven by ammonia-oxidizing microorganisms (DCF_AOB) were studied under various water temperatures and nitrogen concentrations using ¹⁴C labeling (NaH¹⁴CO₃) and the allylthiourea (ATU) inhibitor method. The Yangtze River Estuary was used as a study area and sampling locations were set up in the estuary and offshore locations. The DCF rates in the Yangtze River Estuary ranged from 0.23 to 0.33 μmolC·L^–1·d^–1 and that DCF_AOB rates accounted for 4.13% to 43.61% of the DCF. Although DCF rates increase significantly under optimum temperatures, the increase was more obvious with changes in ambient temperature under low salinity. The optimum temperatures for DCF in areas of low and high salinity were found to be 30℃ and 25℃, respectively, with the addition of ammonia-nitrogen at these conditions significantly increasing the DCF rates. The results of this study reveal how dark carbon fixation in estuarine water can change when subjected to environmental temperature changes, thereby providing theoretical support and data references to aid in the comprehensive understanding and scientific assessment of carbon fixation and carbon sink flux in estuarine ecosystems.

Key words: dark carbon fixation, the Yangtze River Estuary, ammonia-oxidizing microorganisms, salinity

CLC Number:

X142

Jiaming CHEN, Shiming WANG, Rongrong YANG, Ziyan CHEN, Xia LIANG, Lijun HOU. Temperature adaptability of dark carbon fixation in seawater fromthe Yangtze River Estuary[J]. Journal of East China Normal University(Natural Science), 2024, 2024(1): 104-112.

Figures/Tables 5

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Table 1

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References 44

1	TURNER R E, RABALAIS N N.. Coastal eutrophication near the Mississippi river delta. Nature, 1994, 368 (6742): 619- 621.
2	VASQUEZ-CARDENAS D, MEYSMAN F J R, BOSCHKER H T S. A cross-system comparison of dark carbon fixation in coastal sediments [J]. Global Biogeochemical Cycles, 2020, 34(2): e2019GB006298.
3	BALTAR F, HERNDL G J.. Ideas and perspectives: Is dark carbon fixation relevant for oceanic primary production estimates?. Biogeosciences, 2019, 16 (19): 3793- 3799.
4	MIDDELBURG J J.. Chemoautotrophy in the ocean. Global Biogeochemical Cycles, 2011, 38 (24): 94- 97.
5	ZHANG Y, QIN W, HOU L, et al.. Nitrifier adapation to low energy flux controls inventory of reduced nitrogen in the dark ocean. PNAS, 2020, 117 (9): 4823- 4830.
6	LIU B L, HOU L J, ZHENG Y, et al.. Dark carbon fixation in intertidal sediments: Controlling factors and driving microorganisms. Water Research, 2022, 216, 118381.
7	ARNDT S, JORGENSEN B B, LAROWE D E, et al.. Quantifying the degradation of organic matter in marine sediments: A review and synthesis. Earth-Science Reviews, 2013, 123 (4): 53- 86.
8	LEE D Y, OWENS M S, CRUMP B C, et al.. Elevated microbial CO₂ production and fixation in the oxic/anoxic interface of estuarine water columns during seasonal anoxia. Estuarine, Coastal and Shelf Science, 2015, 164 (5): 65- 76.
9	SEVERIN I, CONFURIUS-GUNS V, STAL L J.. Effect of salinity on nitrogenase activity and composition of the active diazotrophic community in intertidal microbial mats. Archives of Microbiology, 2012, 194 (6): 483- 491.
10	SANTOS J P, MENDES D, MONTEIRO M, et al.. Salinity impact on ammonia oxidizers activity and amoA expression in estuarine sediments. Estuarine, Coastal and Shelf Science, 2018, 211, 177- 187.
11	ZHANG Y, CHEN L J, DAI T J, et al.. The influence of salinity on the abundance, transcriptional activity, and diversity of AOA and AOB in an estuarine sediment: A microcosm study. Applied Microbiology and Biotechnology, 2015, 99, 9825- 9833.
12	GALAZZO F B, CRICHTON K A, BARKER S, et al.. Temperature dependency of metabolic rates in the upper ocean: A positive feedback to global climate change?. Global and Planetary Change, 2018, 170 (9): 201- 212.
13	AKINYEDE R, TAUBERT M, SCHRUMPF M, et al.. Temperature sensitivity of dark CO₂ fixation in temperate forest soils. Biogeosciences, 2022, 19 (17): 4011- 4028.
14	NEL J A, CRAMER M D.. Soil microbial anaplerotic CO₂ fixation in temperate soils. Geoderma, 2019, 335, 170- 178.
15	QIN W, MARTENS-HABBENA W, AMIN S A, et al.. Marine ammonia-oxidizing archaeal isolates display obligate mixotrophy and wide ecotypic variation. Proceedings of the National Academy of Sciences, 2014, 111 (34): 12504- 12509.
16	郑珍珍. 海洋氨氧化过程对温度的响应 [D]. 福建厦门: 厦门大学, 2018.
17	MASSON-DELMOTTE V P, ZHAI A, PIRANI S L, et al. Contribution of Working Group I to the sixth assessment report of the intergovernmental panel on climate change [C]// IPCC Climate Change 2021: The Physical Science Basis. Cambridge: Cambridge University Press, 2021.
18	LIN X, HOU L, LIU M, et al.. Nitrogen mineralization and immobilization in sediments of the East China Sea: Spatiotemporal variations and environmental implications. Journal of Geophysical Research: Biogeosciences, 2016, 121 (11): 2842- 2855.
19	LIU H, HE Q, WANG Z, et al.. Dynamics and spatial variability of near-bottom sediment exchange in the Yangtze Estuary, China. Estuarine, Coastal and Shelf Science, 2010, 86 (3): 322- 330.
20	ZHENG Y, JIANG X, HOU L, et al.. Shifts in the community structure and activity of anaerobic ammonium oxidation bacteria along an estuarine salinity gradient. Journal of Geophysical Research: Biogeosciences, 2016, 121 (6): 1632- 1645.
21	买佳阳, 蒋雪中.. 2000年以来长江河口海表温度变化MODIS分析. 遥感学报, 2015, 19 (5): 818- 826.
22	王燕, 姚振童, 祝艳君, 等.. 2019年渤海氮磷营养盐季节变化及富营养化状况. 海洋环境科学, 2021, 40 (6): 915- 921.
23	PENG X, FUCHSMAN C A, WARD B B, et al.. Ammonia and nitrite oxidation in the Eastern Tropical North Pacific. Global Biogeochemical Cycles, 2015, 29 (12): 2034- 2049.
24	BERG C, VANDIEKEN V, THAMDRUP B, et al.. Significance of archaeal nitrification in hypoxic waters of the Baltic Sea. ISME Journal, 2014, 9 (6): 1319- 1332.
25	LASSEN M K, NIELSEN K D, RICHARDSON K, et al.. The effects of temperature increase on a temperate phytoplankton community: A mesocosm climate change scenario. Journal of Experimental Marine Biology and Ecology, 2010, 383 (1): 79- 88.
26	TAUCHER J, SCHULZ K G, DITTMAR T, et al.. Enhanced carbon overconsumption in response to increasing temperatures during a mesocosm experiment. Biogeosciences, 2012, 9 (9): 3531- 3544.
27	YVON-DUROCHER G, ALLEN A P, CELLAMARE M, et al.. Five years of experimental warming increases the biodiversity and productivity of phytoplankton. PLoS Biology, 2015, 13 (12): e1002324.
28	FANG C, SMITH P, MONCRIEFF J B, et al.. Similar response of labile and resistant soil organic matter pools to changes in temperature. Nature, 2015, 433 (7021): 57- 59.
29	HICKS PRIES C E, CASTANHA C, PORRAS R, et al.. The whole-soil carbon flux in response to warming. Science, 2017, 355 (6332): 1420- 1423.
30	HELDER W, VRIES R T P D.. Estuarine nitrite maxima and nitrifying bacteria. Netherlands Journal of Sea Research, 1983, 17 (1): 1- 18.
31	GROENEWEG J, SELLNER B, TAPPE W.. Ammonia oxidation in nitrosomonas at NH₃ concentrations near k_m: Effects of pH and temperature. Water Research, 1994, 28 (2): 2561- 2566.
32	GAO J, HOU L J, ZHENG Y L, et al.. Shifts in the community dynamics and activity of ammonia-oxidizing prokaryotes along the Yangtze estuarine salinity gradient. Journal of Geophysical Research: Biogeosciences, 2018, 123, 3458- 3469.
33	WEI H C, LIN X B.. Shifts in the relative abundance and potential rates of sediment ammonia-oxidizing archaea and bacteria along environmental gradients of an urban river–estuary–adjacent sea continuum. Science of the Total Environment, 2021, 771, 144824.
34	ZHANG Y, XIE X, JIAO N, et al.. Diversity and distribution of amoA-type nitrifying and nirS-type denitrifying microbial communities in the Yangtze River Estuary. Biogeosciences, 2014, 11 (8): 2131- 2145.
35	李奕燃, 于雪, 李晓强, 等.. 利用16S rRNA高通量测序技术考察温度对生物脱氮硝化过程中亚硝酸盐氧化菌代谢功能的影响. 环境工程学报, 2022, 16 (3): 980- 988.
36	TAYLOR A E, MELLBYE B L.. Differential responses of the catalytic efficiency of ammonia and nitrite oxidation to changes in temperature. Frontiers in Microbiology, 2022, 13, 817986.
37	GUNDUZ S, DEKA D J, OZKAN U S.. A review of the current trends in high-temperature electrocatalytic ammonia production using solid electrolytes. Journal of Catalysis, 2020, 387, 207- 216.
38	ALONSO-SÁEZ L, CASAMAYOR E O, BERTILSSON S, et al.. High bicarbonate assimilation in the dark by Arctic bacteria. The ISME Journal, 2010, (4): 1581- 1590.
39	LIU Y, YAO T, JIAO N, et al. Salinity impact on bacterial community composition in five high-altitude lakes from the Tibetan Plateau, Western China [J]. Geomicrobiology Journal, 2013(12), 30: 462–469.
40	ZHONG Z P, LIU Y, MIAO L L, et al.. Prokaryotic community structure driven by salinity and ionic concentrations in plateau lakes of the Tibetan Plateau. Applied and Environmental Microbiology, 2016, 82 (5): 1846- 1858.
41	YUE L, KONG W, JI M, et al.. Community response of microbial primary producers to salinity is primarily driven by nutrients in lakes. Science of the Total Environment, 2019, 696 (6): 134001.
42	LOZUPONE C A, KNIGHT R.. Global patterns in bacterial diversity. Proceedings of the National Academy of Sciences of the United States of America, 2007, 104 (27): 11436- 11440.
43	ASHRAF M, HARRIS P J C.. Photosynthesis under stressful environments: An overview. Photosynthetica, 2013, 51, 163- 190.
44	HARPOLE W S, NGAI J T, CLELAND E E, et al.. Nutrient co-limitation of primary producer communities. Ecology Letters, 2011, 14 (9): 852- 862.

温度/℃	不同${\rm{NH}}_4^+ $添加处理组
温度/℃	空白组	5.0 μmol·L^–1	10.0 μmol·L^–1	15.0 μmol·L^–1
20
25
30
35
40

采样断面	水体温度/℃	盐度/‰	${\rm{NH}}_4^+ $浓度/(μmol·L^–1)	${\rm{NO}}_3^- $浓度/(μmol·L^–1)	${\rm{NO}}_2^- $浓度/(μmol·L^–1)	DIC浓度/(mmol·L^–1)
近岸	28.5 ± 0.2	1.1 ± 0.01**	1.06 ± 0.29	107 ± 0.55**	0.09 ± 0.02*	1.73 ± 0.01*
近海	28.3 ± 0.1	32.6 ± 2.9**	0.67 ± 0.01	3.55 ± 1.90**	0.25 ± 0.07*	2.08 ± 0.16*

生态过程	区域	样本	培养温度/℃	Q₁₀	参考文献
暗碳固定	长江口	水体	20、30	1.1 ~ 2.5	本研究
	德国中部森林	山毛榉土壤	4、14	1.81 ± 0.17	Akinyede等^[13]
	德国中部森林	云杉土壤	4、14	2.07 ± 0.34	Akinyede等^[13]
氨氧化	埃姆斯多拉德河口	AOB	10、20	3.3	Helder等^[30]
氨氧化	普吉特湾河口	AOA	10、20	2.5 ~ 2.9	Qin等^[15]
呼吸	温带针叶林	土壤	4	2.4	Hicks等^[29]

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