Biocrusts impact niche separation of ammonia oxidizing microorganisms in the Gurbantunggut Desert, northwestern China

doi:10.17520/biods.2019415

Abstract

Abstract:

Aims: Biological soil crusts (Biocrusts) are complex assemblages of lichens, bryophytes, cyanobacteria, fungi, and heterotrophic microbial organisms in the top few centimetres of desert soils. Biocrusts perform important ecological roles in the nitrogen cycle of desert ecosystems. In desert ecosystems, water sources are vital, and the seasonal melting snow in early spring resurrects biocrusts in the Gurbantunggut desert and begins nitrogen fixation. However, little is known about how biocrusts impact nitrifier distributions across the landscape, specifically ammonia oxidation archaea (AOA) and ammonia oxidation bacteria (AOB).
Methods: We used fluorescent quantative PCR (qPCR) methods to characterize AOA and AOB amoA gene abundances at different soil depths (0-2, 2-5, 5-10 and 10-20 cm) in biocrust and biocrust-removal soils. Desert nitrification potential and soil physicochemical parameters were researched to understand biocrust impacts on the desert soil nitrogen cycle.
Results: The AOA amoA gene abundance was remarkably larger than that of AOB across all soil samples. ANOVA results showed that biocrusts significantly affected AOA and AOB amoA gene abundance (P < 0.01) while PNR results indicated that biocrust removal significantly reduced soil nitrification potential (P < 0.001), which confirmed that biocrusts play an important role in regulating nitrogen transformation in the Gurbantunggut desert. A redundancy analysis confirmed that soil moisture and NH₄ ⁺-N were the key environmental factors affecting niche separation of AOA and AOB in desert soil.
Conclusion: Biocrusts coupled with oil moisture and NH₄⁺-N affected differential distribution of ammonia oxidizing microorganisms in the temperate desert in the early spring.

Key words: biological soil crsut, snowmelt period, ammonia-oxidizing microbes, desert soil, nitrogen transformation

Xin Liu, Xiaoying Rong, Yuanming Zhang. Biocrusts impact niche separation of ammonia oxidizing microorganisms in the Gurbantunggut Desert, northwestern China[J]. Biodiv Sci, 2021, 29(1): 43-52.

Add to citation manager EndNote|Ris|BibTeX

URL: https://www.biodiversity-science.net/EN/10.17520/biods.2019415

https://www.biodiversity-science.net/EN/Y2021/V29/I1/43

Figures/Tables 6

References 52

[1]	Adair KL, Schwartz E (2008) Evidence that ammonia-oxidizing Archaea are more abundant than ammonia-oxidizing bacteria in semiarid soils of northern Arizona, USA. Microbial Ecology, 56, 420-426. URL PMID
[2]	Belnap J (1996) Soil surface disturbances in cold deserts: Effects on nitrogenase activity in cyanobacterial-lichen soil crusts. Biology and Fertility of Soils, 23, 362-367.
[3]	Belnap J (2002) Impacts of off-road vehicles on nitrogen cycles in biological soil crusts: Resistance in different U. S. deserts. Journal of Arid Environments, 52, 155-165.
[4]	Belnap J (2003) The world at your feet: Desert biological soil crusts. Frontiers in Ecology and the Environment, 1, 181-189.
[5]	Belnap J, Phillips SL, Miller ME (2004) Response of desert biological soil crusts to alterations in precipitation frequency. Oecologia, 141, 306-316. URL PMID
[6]	Condon LA, Pyke DA (2018) Resiliency of biological soil crusts and vascular plants varies among morphogroups with disturbance intensity. Plant and Soil, 433, 271-287.
[7]	Delgado-Baquerizo M, Maestre FT, Eldridge DJ, Singh BK (2016) Microsite differentiation drives the abundance of soil ammonia oxidizing bacteria along aridity gradients. Frontiers in Microbiology, 7, 505.
[8]	Di HJ, Cameron KC, Shen JP, Winefield CS, O’Callaghan M, Bowatte S, He JZ (2010) Ammonia-oxidizing bacteria and archaea grow under contrasting soil nitrogen conditions. FEMS Microbiology Ecology, 72, 386-394. URL PMID
[9]	Eldridge DJ, Freudenberger D, Koen TB (2006) Diversity and abundance of biological soil crust taxa in relation to fine and coarse-scale disturbances in a grassy eucalypt woodland in Eastern Australia. Plant and Soil, 281, 255-268.
[10]	Eldridge DJ, Soliveres S, Bowker MA, Val J (2013) Grazing dampens the positive effects of shrub encroachment on ecosystem functions in a semi-arid woodland. Journal of Applied Ecology, 50, 1028-1038.
[11]	Erguder TH, Boon N, Wittebolle L, Marzorati M, Verstraete W (2009) Environmental factors shaping the ecological niches of ammonia-oxidizing archaea. FEMS Microbiology Reviews, 33, 855-869.
[12]	Ferrenberg S, Reed SC, Belnap J (2015) Climate change and physical disturbance cause similar community shifts in biological soil crusts. Proceedings of the National Academy of Sciences, USA, 112, 12116-12121.
[13]	Ferrenberg S, Tucker CL, Reed SC (2017) Biological soil crusts: Diminutive communities of potential global importance. Frontiers in Ecology and the Environment, 15, 160-167.
[14]	Francis CA, Roberts KJ, Beman JM, Santoro AE, Oakley BB (2005) Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proceedings of the National Academy of Sciences, USA, 102, 14683-14688.
[15]	Garcia V, Aranibar J, Pietrasiak N (2015) Multiscale effects on biological soil crusts cover and spatial distribution in the Monte Desert. Acta Oecologica, 69, 35-45.
[16]	Garcia-Pichel F, Johnson SL, Youngkin D, Belnap J (2003) Small-scale vertical distribution of bacterial biomass and diversity in biological soil crusts from arid lands in the Colorado Plateau. Microbial Ecology, 46, 312-321. URL PMID
[17]	Hu BL, Liu S, Wang W, Shen LD, Lou LP, Liu WP, Tian GM, Xu XY, Zheng P (2014) pH-dominated niche segregation of ammonia-oxidising microorganisms in Chinese agricultural soils. FEMS Microbiology Ecology, 90, 290-299.
[18]	Hu R, Wang XP, Pan YX, Zhang YF, Zhang H, Chen N (2015) Seasonal variation of net N mineralization under different biological soil crusts in Tengger Desert, North China. CATENA, 127, 9-16.
[19]	Johnson SL, Budinoff CR, Belnap J, Garcia-Pichel F (2005) Relevance of ammonium oxidation within biological soil crust communities. Environmental Microbiology, 7, 1-12.
[20]	Johnson SL, Neuer S, Garcia-Pichel F (2007) Export of nitrogenous compounds due to incomplete cycling within biological soil crusts of arid lands. Environmental Microbiology, 9, 680-689.
[21]	Coe KK, Belnap J, Sparks JP (2012) Precipitation-driven carbon balance controls survivorship of desert biocrust mosses. Ecology, 93, 1626-1636. DOI URL PMID
[22]	Kowalchuk GA, Stephen JR (2001) Ammonia-oxidizing bacteria: A model for molecular microbial ecology. Annual Review of Microbiology, 55, 485-529. URL PMID
[23]	Kurola J, Salkinoja-Salonen M, Aarnio T, Hultman J, Romantschuk M (2005) Activity, diversity and population size of ammonia-oxidising bacteria in oil-contaminated landfarming soil. FEMS Microbiology Letters, 250, 33-38. DOI URL PMID
[24]	Leininger S, Urich T, Schloter M, Schwark L, Qi J, Nicol GW, Prosser JI, Schuster SC, Schleper C (2006) Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature, 442, 806-809. URL PMID
[25]	Liu JJ, Yu ZH, Yao Q, Sui YY, Shi Y, Chu HY, Tang CX, Franks AE, Jin J, Liu XB, Wang GH (2018) Ammonia-oxidizing archaea show more distinct biogeographic distribution patterns than ammonia-oxidizing bacteria across the black soil zone of Northeast China. Frontiers in Microbiology, 9, 171. URL PMID
[26]	Liu RY, Li K, Zhang HX, Zhu JG, Joshi D (2014) Spatial distribution of microbial communities associated with dune landform in the Gurbantunggut Desert, China. Journal of Microbiology, 52, 898-907.
[27]	MagalhÃ£es CM, Machado A, Frank-Fahle B, Lee CK, Cary SC (2014) The ecological dichotomy of ammonia-oxidizing archaea and bacteria in the hyper-arid soils of the Antarctic Dry Valleys. Frontiers in Microbiology, 5, 515. DOI URL PMID
[28]	Marusenko Y, Bates ST, Anderson I, Johnson SL, Soule TY, Garcia-Pichel F (2013) Ammonia-oxidizing archaea and bacteria are structured by geography in biological soil crusts across North American arid lands. Ecological Processes, 2, 1-10.
[29]	Matzner E, Borken W (2008) Do freeze-thaw events enhance C and N losses from soils of different ecosystems? A review. European Journal of Soil Science, 59, 274-284.
[30]	Prosser JI, Nicol GW (2012) Archaeal and bacterial ammonia-oxidisers in soil: The quest for niche specialisation and differentiation. Trends in Microbiology, 20, 523-531. DOI URL PMID
[31]	Rotthauwe JH, Witzel KP, Liesack W (1997) The ammonia monooxygenase structural gene amoA as a functional marker: Molecular fine-scale analysis of natural ammonia-oxidizing populations. Applied and Environmental Microbiology, 63, 4704-4712. DOI URL PMID
[32]	Ferrenberg S, Reed SC, Belnap J (2015) Climate change and physical disturbance cause similar community shifts in biological soil crusts. Proceedings of the National Academy of Sciences, USA, 112, 12116-12121.
[33]	Steinweg JM, Fisk MC, McAlexander B, Groffman PM, Hardy JP (2008) Experimental snowpack reduction alters organic matter and net N mineralization potential of soil macroaggregates in a northern hardwood forest. Biology and Fertility of Soils, 45, 1-10.
[34]	Stempfhuber B, Engel M, Fischer D, Neskovic-Prit G, Wubet T, Schöning I, Gubry-Rangin C, Kublik S, Schloter-Hai B, Rattei T, Welzl G, Nicol GW, Schrumpf M, Buscot F, Prosser JI, Schloter M (2015) pH as a driver for ammonia-oxidizing archaea in forest soils. Microbial Ecology, 69, 879-883. URL PMID
[35]	Tao JJ, Bai TS, Xiao R, Wang P, Wang FW, Duryee AM, Wang Y, Zhang Y, Hu SJ (2018) Vertical distribution of ammonia-oxidizing microorganisms across a soil profile of the Chinese Loess Plateau and their responses to nitrogen inputs. Science of The Total Environment, 635, 240-248.
[36]	Valentine DL (2007) Adaptations to energy stress dictate the ecology and evolution of the Archaea. Nature Reviews Microbiology, 5, 316-323. URL PMID
[37]	Verhamme DT, Prosser JI, Nicol GW (2011) Ammonia concentration determines differential growth of ammonia-oxidising archaea and bacteria in soil microcosms. The ISME Journal, 5, 1067-1071. URL PMID
[38]	Weber B, Wu DM, Tamm A, Ruckteschler N, Rodríguez-Caballero E, Steinkamp J, Meusel H, Elbert W, Behrendt T, Sörgel M, Cheng YF, Crutzen PJ, Su H, Pöschl U (2015) Biological soil crusts accelerate the nitrogen cycle through large NO and HONO emissions in drylands. Proceedings of the National Academy of Sciences, USA, 112, 15384-15389.
[39]	Wu L, Zhang YM, Zhang J, Downing A (2015) Precipitation intensity is the primary driver of moss crust-derived CO₂ exchange: Implications for soil C balance in a temperate desert of northwestern China. European Journal of Soil Biology, 67, 27-34.
[40]	Wu N, Zhang YM, Downing A (2009) Comparative study of nitrogenase activity in different types of biological soil crusts in the Gurbantunggut Desert, Northwestern China. Journal of Arid Environments, 73, 828-833.
[41]	Xiao R, Qiu YP, Tao JJ, Zhang XL, Chen HH, Reberg-Horton SC, Shi W, Shew HD, Zhang Y, Hu SJ (2019) Biological controls over the abundances of terrestrial ammonia oxidizers. Global Ecology and Biogeography, 29, 384-399.
[42]	Yao HY, Campbell CD, Chapman SJ, Freitag TE, Nicol GW, Singh BK (2013) Multi-factorial drivers of ammonia oxidizer communities: Evidence from a national soil survey. Environmental Microbiology, 15, 2545-2556. DOI URL PMID
[43]	Zhang BC, Zhang YM, Su YG, Wang JZ, Zhang J (2013) Responses of microalgal-microbial biomass and enzyme activities of biological soil crusts to moisture and inoculated microcoleus vaginatus gradients. Arid Land Research and Management, 27, 216-230.
[44]	Zhang CP, Niu DC, Song ML, Elser JJ, Okie JG, Fu H (2018) Effects of rainfall manipulations on carbon exchange of cyanobacteria and moss-dominated biological soil crusts. Soil Biology and Biochemistry, 124, 24-31.
[45]	Zhang YM, Chen J, Wang L, Wang XQ, Gu ZH (2007) The spatial distribution patterns of biological soil crusts in the Gurbantunggut Desert, Northern Xinjiang, China. Journal of Arid Environments, 68, 599-610.
[46]	Zhao RM, Hui R, Liu LC, Xie M, An LZ (2018) Effects of snowfall depth on soil physical-chemical properties and soil microbial biomass in moss-dominated crusts in the Gurbantunggut Desert, Northern China. CATENA, 169, 175-182.
[47]	Zhou XB, Smith H, Giraldo SA, Belnap J, Garcia-Pichel F (2016) Differential responses of dinitrogen fixation, diazotrophic cyanobacteria and ammonia oxidation reveal a potential warming-induced imbalance of the N-cycle in biological soil crusts. PLoS ONE, 11, e0164932. DOI URL PMID
[48]	Zhou XB, Tao Y, Yin BF, Tucker C, Zhang YM (2020) Nitrogen pools in soil covered by biological soil crusts of different successional stages in a temperate desert in Central Asia. Geoderma, 366, 114166.
[49]	Zhou XB, Zhang YM (2014a) Season and nitrogen effects on activities of three hydrolytic enzymes in soils of the gurbantunggut desert, northwest China. Communications in Soil Science and Plant Analysis, 45, 1699-1713.
[50]	Zhou XB, Zhang YM (2014b) Seasonal pattern of soil respiration and gradual changing effects of nitrogen addition in a soil of the Gurbantunggut Desert, northwestern China. Atmospheric Environment, 85, 187-194.
[51]	Zhou XQ, Chen CR, Wang YF, Xu ZH, Duan JC, Hao YB, Smaill S (2013) Soil extractable carbon and nitrogen, microbial biomass and microbial metabolic activity in response to warming and increased precipitation in a semiarid Inner Mongolian grassland. Geoderma, 206, 24-31.
[52]	Zhuang WW, Downing A, Zhang YM (2015) The influence of biological soil crusts on ¹⁵N translocation in soil and vascular plant in a temperate desert of northwestern China . Journal of Plant Ecology, 8, 420-428.

	温度 Temperature (℃)	含水量 Soil moisture (%)	pH	电导率 Conductivity (μs/cm)	全碳 Total Carbon (mg/g)	全氮 Total Nitrogen (mg/g)
结皮覆盖 Biocrusts
0-2 cm	0.5 ± 0.0 A**	10.63 ± 0.45 A	8.25 ± 0.05 C	4.55 ± 0.26 A	6.72 ± 0.12 A*	0.38 ± 0.02 A**
2-5 cm	0.2 ± 0.0 B*	6.17 ± 0.23 B**	8.37 ± 0.03 B	3.38 ± 0.17 B	5.76 ± 0.17 A	0.23 ± 0.02 B
5-10 cm	0.2 ± 0.0^a B**	3.90 ± 0.12 C	8.55 ± 0.02 A	2.92 ± 0.04 B**	6.74 ± 0.29 A	0.25 ± 0.01 B
10-20 cm	0.1 ± 0.0 B**	2.00 ± 0.21 D	8.57 ± 0.01 A	3.33 ± 0.16 B**	6.47 ± 0.33 A	0.23 ± 0.02 B
去除结皮 Biocrusts-removal
0-2 cm	0.1 ± 0.0 A	10.75 ± 1.54 A	8.43 ± 0.06 A*	3.96 ± 0.53 A	5.86 ± 0.21 A	0.23 ± 0.01 AB
2-5 cm	0.1 ± 0.0 A	4.90 ± 0.21 B	8.44 ± 0.02 A	3.65 ± 0.24 A	5.83 ± 0.39 A	0.27 ± 0.00 A*
5-10 cm	-0.1 ± 0.0^aB	3.65 ± 0.22 B	8.60 ± 0.05 A	2.37 ± 0.13 B	5.82 ± 0.44 A	0.27 ± 0.02 AB
10-20 cm	-0.2 ± 0.0 C	2.48 ± 0.10 B	8.61 ± 0.07 A	2.65 ± 0.06 B	6.04 ± 0.23 A	0.22 ± 0.01 B

	温度 Temperature (℃)	含水量 Soil moisture (%)	pH	电导率 Conductivity (μs/cm)	全碳 Total Carbon (mg/g)	全氮 Total Nitrogen (mg/g)
结皮覆盖 Biocrusts
0-2 cm	0.5 ± 0.0 A**	10.63 ± 0.45 A	8.25 ± 0.05 C	4.55 ± 0.26 A	6.72 ± 0.12 A*	0.38 ± 0.02 A**
2-5 cm	0.2 ± 0.0 B*	6.17 ± 0.23 B**	8.37 ± 0.03 B	3.38 ± 0.17 B	5.76 ± 0.17 A	0.23 ± 0.02 B
5-10 cm	0.2 ± 0.0^a B**	3.90 ± 0.12 C	8.55 ± 0.02 A	2.92 ± 0.04 B**	6.74 ± 0.29 A	0.25 ± 0.01 B
10-20 cm	0.1 ± 0.0 B**	2.00 ± 0.21 D	8.57 ± 0.01 A	3.33 ± 0.16 B**	6.47 ± 0.33 A	0.23 ± 0.02 B
去除结皮 Biocrusts-removal
0-2 cm	0.1 ± 0.0 A	10.75 ± 1.54 A	8.43 ± 0.06 A*	3.96 ± 0.53 A	5.86 ± 0.21 A	0.23 ± 0.01 AB
2-5 cm	0.1 ± 0.0 A	4.90 ± 0.21 B	8.44 ± 0.02 A	3.65 ± 0.24 A	5.83 ± 0.39 A	0.27 ± 0.00 A*
5-10 cm	-0.1 ± 0.0^aB	3.65 ± 0.22 B	8.60 ± 0.05 A	2.37 ± 0.13 B	5.82 ± 0.44 A	0.27 ± 0.02 AB
10-20 cm	-0.2 ± 0.0 C	2.48 ± 0.10 B	8.61 ± 0.07 A	2.65 ± 0.06 B	6.04 ± 0.23 A	0.22 ± 0.01 B

	差异来源 Source	自由度 df	f值 f	Pr > F
氨氧化古菌 AOA amoA	处理 Treatment	1	0.13	0.725
	土层 Layer	3	64.00	< 0.001
	处理 × 土层 Treatment × layer	3	9.45	< 0.001
氨氧化细菌 AOB amoA	处理 Treatment	1	118.85	< 0.001
	土层 Layer	3	128.34	< 0.001
	处理 × 土层 Treatment × layer	3	103.57	< 0.001
潜在硝化速率 PNR	处理 Treatment	1	24.03	< 0.001
	土层 Layer	3	50.81	< 0.001
	处理 × 土层 Treatment × layer	3	8.69	< 0.001

	差异来源 Source	自由度 df	f值 f	Pr > F
氨氧化古菌 AOA amoA	处理 Treatment	1	0.13	0.725
	土层 Layer	3	64.00	< 0.001
	处理 × 土层 Treatment × layer	3	9.45	< 0.001
氨氧化细菌 AOB amoA	处理 Treatment	1	118.85	< 0.001
	土层 Layer	3	128.34	< 0.001
	处理 × 土层 Treatment × layer	3	103.57	< 0.001
潜在硝化速率 PNR	处理 Treatment	1	24.03	< 0.001
	土层 Layer	3	50.81	< 0.001
	处理 × 土层 Treatment × layer	3	8.69	< 0.001

	潜在硝化速率 Potential nitrification rate
	结皮覆盖土壤 Biocrusts soil	去除结皮土壤 Biocrusts-removal soil
氨氧化古菌 AOA	?0.73**	?0.06
氨氧化细菌 AOB	0.88**	0.76**
温度 Tem	0.90**	0.66*
含水量 SM	0.91**	0.87**
pH	?0.79**	?0.44
电导率 Cond	0.75**	0.48
全碳 TC	0.05	0.09
全氮 TN	0.80**	?0.26
铵态氮 NH₄⁺-N	0.93**	0.36
硝态氮 NO₃^--N	?0.60*	?0.08