Moisture and temperature controls on nitrification differ among ammonia oxidizer communities from three alpine soil habitats

doi:10.1007/s11707-015-0556-x

Front. Earth Sci.

2016, Vol. 10

Issue (1) : 1-12 https://doi.org/10.1007/s11707-015-0556-x

RESEARCH ARTICLE

Moisture and temperature controls on nitrification differ among ammonia oxidizer communities from three alpine soil habitats

Brooke B. OSBORNE^1,^2,^*(

),Jill S. BARON^1,³,Matthew D. WALLENSTEIN^1,⁴

1. Natural Resource Ecology Laboratory, Colorado State University, Fort Collins, CO 80523, USA
2. Present address: Department of Ecology and Evolutionary Biology, Brown University, Providence, RI 02912, USA
3. U.S. Geological Survey Fort Collins Science Center, Fort Collins, CO 80526, USA
4. Department of Ecosystem Science and Sustainability, Colorado State University, Fort Collins, CO 80523, USA

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Abstract

Climate change is altering the timing and magnitude of biogeochemical fluxes in many high-elevation ecosystems. The consequent changes in alpine nitrification rates have the potential to influence ecosystem scale responses. In order to better understand how changing temperature and moisture conditions may influence ammonia oxidizers and nitrification activity, we conducted laboratory incubations on soils collected in a Colorado watershed from three alpine habitats (glacial outwash, talus, and meadow). We found that bacteria, not archaea, dominated all ammonia oxidizer communities. Nitrification increased with moisture in all soils and under all temperature treatments. However, temperature was not correlated with nitrification rates in all soils. Site-specific temperature trends suggest the development of generalist ammonia oxidzer communities in soils with greater in situ temperature fluctuations and specialists in soils with more steady temperature regimes. Rapidly increasing temperatures and changing soil moisture conditions could explain recent observations of increased nitrate production in some alpine soils.

Keywords ammonia-oxidizing archaea (AOA) ammonia-oxidizing bacteria (AOB) global change Loch Vale watershed nitrification thermal adaptation

Corresponding Author(s): Brooke B. OSBORNE

Just Accepted Date: 22 October 2015 Online First Date: 16 November 2015 Issue Date: 25 December 2015

Cite this article:

Brooke B. OSBORNE,Jill S. BARON,Matthew D. WALLENSTEIN. Moisture and temperature controls on nitrification differ among ammonia oxidizer communities from three alpine soil habitats[J]. Front. Earth Sci., 2016, 10(1): 1-12.

URL:

https://academic.hep.com.cn/fesci/EN/10.1007/s11707-015-0556-x
https://academic.hep.com.cn/fesci/EN/Y2016/V10/I1/1

Fig.1 Annotated map of the Loch Vale watershed, Rocky Mountain National Park, CO, USA. Soil sampling sites are indicated with red circles.

Fig.2 Soil temperature data for talus (brown lines) and meadow (green lines). Temperatures were recorded at 30-minute intervals by two iButton temperature sensors buried at 5 cm. Temperatures were not collected in outwash soils, which were frozen at the time of sensor installation.

Fig.3 Concentrations of ammonia-oxidizing bacteria (AOB) as well as rates of net nitrification, gross nitrification, and gross NO 3 − consumption measured during laboratory incubations. Outwash data are represented in blue, talus in brown, and meadow in green. Darker bars indicate higher moisture treatments. Asterisks indicate significant differences within soils at P<0.05.

Tab.1 Physical and chemical parameters of Loch Vale soils

Tab.2 Average rates of change in microbial biomass carbon, microbial biomass carbon-specific respiration, and net N mineralization in Loch Vale soils at different temperature and percent water holding capacity treatments

Tab.3 Standardized regression coefficients of multiple regression analyses for net nitrification rates and changes in the abundance of ammonia-oxidizing bacteria

	System	Location	Month, year	NO₃-N /(mg·kg⁻¹)	NH 4 + -N /(mg·kg⁻¹)	DIN/(mg·kg⁻¹)	MBC/(mg·kg⁻¹)	MBN/(mg·kg⁻¹)	References
Outwash	Alpine, primary succession	Colorado (40°17′N, 105°39′W)	July, 2010	0.54–1.5	14–19	15–20	0.05–0.05	BDL	Present study
	Alpine, primary succession	Switzerland (46°28′N, 8°28′E)	July, 2008	0.13–0.23	0.03–0.18	0.16–0.41	58–120	6–19	Brankatschk et al., 2011
	Alpine, high-elevation	Chile (24°43′S, 68°32′W)	Feb., 2009	^a–	–	–	31–58	1.2–2.2	Lynch et al., 2012
	Antarctic Dry Valley	Antarctica (77°37′S, 163°15′'E)	Jan., 2002	4.9	0.09	–	26	4.4	Ball et al., 2009
Talus	Alpine, talus	Colorado (40°17′N, 105°39′W)	July, 2010	1.8–2.3	12–15	14–17	0.34–0.51	0.07–0.07	Present study
	Alpine, talus	Colorado (40°03′N, 105°35′W)	July, 1997–1998	–	–	–	0.028–39	–	Ley et al., 2001
	Alpine, talus	Colorado (40°03′N, 105°35′W)	July, 1995	1–1.7	1.5–5.9	2.5 – 6.9	–	3.1 – 12	Williams et al., 1997
	Alpine, talus	Colorado (40°03′N, 105°35′W)	July, 1996	0.42–0.63	1.5–5.9	2–6.6	–	–	Bieber et al., 1998
	Alpine, dry meadow	Colorado (40°03′N, 105°35′W)	June−Oct., 1992	–	~ 8–15	–	–	~ 100–127	Fisk & Schmidt, 1996
	Alpine, dry meadow	California (multiple sites)	Oct., 2003	~ 0.4–0.83	–	~ 0.56–6.8	~ 942–1500	~ 43–65	Miller et al., 2007
	Alpine, lichen heath	Russia (43°27′N, 41°41′E)	Aug., 1999–2001	0.6–1.6	7–19	8.6–20	–	~ 50–70	Makarov et al., 2003
Meadow	Alpine, wet meadow	Colorado (40°17′N, 105°39′W)	July, 2010	0.7–3.2	20–23	20–25	6.6–11	0.38–0.74	Present study
	Alpine, developed soils	Switzerland (46°28′N, 8°28′E)	July, 2008	0.81–1.3	6.7–13	7.5–14	240–900	29–120	Brankatschk et al., 2011
	Low arctic Tundra	Canada (64°52′N, 111°35′W)	June, 2007	BDL–1.2	0.15–13	0.15–14	7,400–12,000	770–960	Chu & Grogan, 2009
	High arctic	Canada (multiple sites)	July, 2006	0.89–4.5	0.74–5.3	1.6–9.8	–	–	Banerjee et al., 2011

Tab.4 Comparison of soil and microbial parameters in Loch Vale soils and other alpine and arctic study sites

Tab.5 Comparison of net nitrification and nitrogen mineralization rates in Loch Vale soils and other alpine and arctic study sites

1	Alves R J E, Wanek W, Zappe A, Richter A, Svenning M M, Schleper C, Urich T (2013). Nitrification rates in Arctic soils are associated with functionally distinct populations of ammonia-oxidizing archaea. ISME J, 7(8): 1620–1631 https://doi.org/10.1038/ismej.2013.35
2	Baron J S (1992). Biogeochemistry of a Subalpine Ecosystem: Loch Vale Watershed. New York: Springer-Verlag
3	Baron J S, Driscoll C T, Stoddard J L, Richer E E (2011). Empirical critical loads of atmospheric nitrogen deposition for nutrient enrichment and acidification of sensitive US lakes. BioScience, 61(8): 602–613 https://doi.org/10.1525/bio.2011.61.8.6
4	Baron J S, Rueth H M, Wolfe A M, Nydick K R, Allstott E J, Minear J T, Moraska B (2000). Ecosystem responses to nitrogen deposition in the Colorado Front Range. Ecosystems, 3(4): 352–368 https://doi.org/10.1007/s100210000032
5	Baron J S, Schmidt T M, Hartman M D (2009). Climate-induced changes in high elevation stream nitrate dynamics. Glob Change Biol, 15(7): 1777–1789 https://doi.org/10.1111/j.1365-2486.2009.01847.x
6	Bieber A J, Williams M W, Johnsson M J, Davinroy T C (1998). Nitrogen transformations in alpine talus fields, Green Lakes Valley, Front Range, Colorado, USA. Arctic and alpine research, 30(3): 266–271 https://doi.org/10.2307/1551974
7	Boyd E S, Lange R K, Mitchell A C, Havig J R, Hamilton T L, Lafrenière M J, Shock E L, Peters J W, Skidmore M (2011). Diversity, abundance, and potential activity of nitrifying and nitrate-reducing microbial assemblages in a subglacial ecosystem. Appl Environ Microbiol, 77(14): 4778–4787 https://doi.org/10.1128/AEM.00376-11
8	Brankatschk R, Töwe S, Kleineidam K, Schloter M, Zeyer J (2011). Abundances and potential activities of nitrogen cycling microbial communities along a chronosequence of a glacier forefield. ISME J, 5(6): 1025–1037 https://doi.org/10.1038/ismej.2010.184
9	Campbell D H, Kendall C, Chang C C Y, Silva S R, Tonnessen K A (2002). Pathways for nitrate release from an alpine watershed: determination using δ15N and δ18O. Water Resour Res, 38(5): 10-1–10-9 https://doi.org/10.1029/2001WR000294
10	Cannone N, Diolaiuti G, Guglielmin M, Smiraglia C (2008). Accelerating climate change impacts on alpine glacier forefield ecosystems in the European Alps. Ecol Appl, 18(3): 637–648 https://doi.org/10.1890/07-1188.1
11	Chu H, Grogan P (2010). Soil microbial biomass, nutrient availability and nitrogen mineralization potential among vegetation-types in a low arctic tundra landscape. Plant and Soil, 329(1–2): 411–420 https://doi.org/10.1007/s11104-009-0167-y
12	Clow D W (2010). Changes in the timing of snowmelt and streamflow in Colorado: a response to recent warming. J Clim, 23(9): 2293–2306 https://doi.org/10.1175/2009JCLI2951.1
13	Delgado-Baquerizo M, Gallardo A, Wallenstein M D, Maestre F T (2013). Vascular plants mediate the effects of aridity and soil properties on ammonia-oxidizing bacteria and archaea. FEMS Microbiol Ecol, 85(2): 273–282 https://doi.org/10.1111/1574-6941.12119
14	Di H J, Cameron K C, Shen J P, Winefield C S, O’Callaghan M, Bowatte S, He J Z (2010). Ammonia-oxidizing bacteria and archaea grow under contrasting soil nitrogen conditions. FEMS Microbiol Ecol, 72(3): 386–394 https://doi.org/10.1111/j.1574-6941.2010.00861.x
15	Elser J J, Andersen T, Baron J S, Bergström A K, Jansson M, Kyle M, Nydick K R, Steger L, Hessen D O (2009). Shifts in lake N:P stoichiometry and nutrient limitation driven by atmospheric nitrogen deposition. Science, 326(5954): 835–837 https://doi.org/10.1126/science.1176199
16	Erguder T H, Boon N, Wittebolle L, Marzorati M, Verstraete W (2009). Environmental factors shaping the ecological niches of ammonia-oxidizing archaea. FEMS Microbiol Rev, 33(5): 855–869 https://doi.org/10.1111/j.1574-6976.2009.00179.x
17	Fierer N, Schimel J P, Holden P A (2003). Variations in microbial community composition through two soil depth profiles. Soil Biol Biochem, 35(1): 167–176 https://doi.org/10.1016/S0038-0717(02)00251-1
18	Firestone M K, Davidson E A (1989). Microbiological basis of NO and N2O production and consumption in soil. In: Andreae M O, Schimel D S, eds. Exchange of Trace Gases between Terrestrial Ecosystems and the Atmosphere. New York: John Wiley and Sons Ltd, 7–21
19	Fisk M C, Schmidt S K (1996). Microbial responses to nitrogen additions in alpine tundra soil. Soil Biol Biochem, 28(6): 751–755 https://doi.org/10.1016/0038-0717(96)00007-7
20	Fountain A G, Campbell J L, Schuur E A G, Stammerjohn S E, Williams M W, Ducklow H W (2012). The disappearing cryosphere: impacts and ecosystem responses to rapid cryosphere loss. BioScience, 62(4): 405–415 https://doi.org/10.1525/bio.2012.62.4.11
21	Francis C A, Roberts K J, Beman J M, Santoro A E, Oakley B B (2005). Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proc Natl Acad Sci USA, 102(41): 14683–14688 https://doi.org/10.1073/pnas.0506625102
22	Gee G W, Bauder J W (1986). Particle-size analysis. In: Klute A, ed. Methods of Soil Analysis. Part 1. Physical and Mineralogical Methods. Madison: ASA and SSSA Publ, 383–411
23	Gubry-Rangin C, Hai B, Quince C, Engel M, Thomson B C, James P, Schloter M, Griffiths R I, Prosser J I, Nicol G W (2011). Niche specialization of terrestrial archaeal ammonia oxidizers. Proc Natl Acad Sci USA, 108(52): 21206–21211 https://doi.org/10.1073/pnas.1109000108
24	Hannah D M, Brown L E, Milner A M, Gurnell A M, McGregor G R, Petts G E, Smith B P G, Snook D L (2007). Integrating climate-hydrology-ecology for alpine river systems. Aquatic Conservation: Marine and Freshwater Ecosystems, 17(6): 636–656 https://doi.org/10.1002/aqc.800
25	Hatzenpichler R (2012). Diversity, physiology, and niche differentiation of ammonia-oxidizing archaea. Appl Environ Microbiol, 78(21): 7501–7510 https://doi.org/10.1128/AEM.01960-12
26	Huber E, Bell T L, Simpson R R, Adams M A (2011). Relationships among micoclimate, edaphic conditions, vegetarian distribution and soil nitrogen dynamics on the Bogong High Plains, Australia. Austral Ecology, 36(2): 142–152 https://doi.org/10.1111/j.1442-9993.2010.02128.x
27	IPCC (2014). Climate Change, Adaptation, and Vulnerability
28	Kattelmann R, Elder K (1991). Hydrologic characteristics and water balance of an alpine basin in the Sierra Nevada. Water Resour Res, 27(7): 1553–1562 https://doi.org/10.1029/90WR02771
29	Kirkham D, Bartholomew W V (1954). Equations for following nutrient transformations in soil, utilizing tracer data. Soil Sci Soc Am J, 18(1): 33–34 https://doi.org/10.2136/sssaj1954.03615995001800010009x
30	Leininger S, Urich T, Schloter M, Schwark L, Qi J, Nicol G W, Prosser J I, Schuster S C, Schleper C (2006). Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature, 442(7104): 806–809 https://doi.org/10.1038/nature04983
31	Linn D M, Doran J W (1984). Effect of water-filled pore space on carbon dioxide and nitrous oxide production in tilled and nontilled soils. Soil Sci Soc Am J, 48(6): 1267–1272 https://doi.org/10.2136/sssaj1984.03615995004800060013x
32	Lipson D A, Monson R K, Schmidt S K, Weintraub M N (2009). The trade-off between growth rate and yield in microbial communities and the consequences for under-snow soil respiration in a high elevation coniferous forest. Biogeochemistry, 95(1): 23–25 https://doi.org/10.1007/s10533-008-9252-1
33	Makarov M I, Glaser B, Zech W, Malysheva T I, Bulatnikova I V, Volkov A V (2003). Nitrogen dynamics in alpine ecosystems of the northern Caucasus. Plant and Soil, 256(2): 389–402 https://doi.org/10.1023/A:1026134327904
34	Martens-Habbena W, Berube P M, Urakawa H, de la Torre J R, Stahl D A (2009). Ammonia oxidation kinetics determine niche separation of nitrifying Archaea and Bacteria. Nature, 461(7266): 976–979 https://doi.org/10.1038/nature08465
35	Miller A E, Schimel J P, Sickman J O, Meixner T, Doyle A P, Melack J M (2007). Mineralization responses at near-zero temperatures in three alpine soils. Biogeochemistry, 84(3): 233–245 https://doi.org/10.1007/s10533-007-9112-4
36	Morris K H, Mast M A, Clow D W, Wetherbee G A, Baron J S, Taipale C, Gay D, Richer E (2012). 2010 monitoring and tracking wet nitrogen deposition in Rocky Mountain National Park. National Park Service Natural Resource Report, 34
37	Ohtonen R, Fritze H, Pennanen T, Jumpponen A, Trappe J (1999). Ecosystem properties and microbial community changes in primary succession on a glacier forefront. Oecologia, 119(2): 239–246 https://doi.org/10.1007/s004420050782
38	Parton W J, Mosier A R, Ojima D S, Valentine D W, Schimel D S, Weier K, Kulmala A E (1996). Generalized model for N2 and N2O production from nitrification and denitrification. Global Biogeochem Cycles, 10(3): 401–412 https://doi.org/10.1029/96GB01455
39	Prosser J I, Nicol G W (2008). Relative contributions of archaea and bacteria to aerobic ammonia oxidation in the environment. Environ Microbiol, 10(11): 2931–2941 https://doi.org/10.1111/j.1462-2920.2008.01775.x
40	Rango A, van Katwijk V F (1990). Climate change effects on the snowmelt hydrology of western North American mountain basins. Geoscience and Remote Sensing. IEEE Transactions, 28(5): 970–974
41	Rotthauwe J H, Witzel K P, Liesack W (1997). The ammonia monooxygenase structural gene amoA as a functional marker: molecular fine-scale analysis of natural ammonia-oxidizing populations. Appl Environ Microbiol, 63(12): 4704–4712
42	Seastedt T R, Bowman W D, Caine T N, McKnight D, Townsend A, Williams M W (2004). The landscape continuum: a model for high-elevation ecosystems. BioScience, 54(2): 111–121 https://doi.org/10.1641/0006-3568(2004)054[0111:TLCAMF]2.0.CO;2
43	Sickman J O, Leydecker A L, Chang C C Y, Kendall C, Melack J M, Lucero D M, Schimel J (2003). Mechanisms underlying export of N from high-elevation catchments during seasonal transitions. Biogeochemistry, 64(1): 1–24 https://doi.org/10.1023/A:1024928317057
44	Stark J M, Hart S C (1996). Diffusion technique for preparing salt solutions, Kjeldahl digests, and persulfate digests for nitrogen-15 analysis. Soil Sci Soc Am J, 60(6): 1846–1855 https://doi.org/10.2136/sssaj1996.03615995006000060033x
45	Sun G, Luo P, Wu N, Qiu P F, Gao Y H, Chen H, Shi F S (2009). Stellera chamaejasme L. increases soil N availability, turnover rates and microbial biomass in an alpine meadow ecosystem on the eastern Tibetan Plateau of China. Soil Biology & Biochemistry, 41(1): 86–91 https://doi.org/10.1016/j.soilbio.2008.09.022
46	Tai X S, Mao W L, Liu G X, Chen T, Zhang W, Wu X K, Long H Z, Zhang B G, Gao T P (2014). Distribution of ammonia oxidizers in relation to vegetation characteristics in the Qilian Mountains, northwestern China. Biogeosciences Discuss, 11(4): 5123–5146 https://doi.org/10.5194/bgd-11-5123-2014
47	Valentine D L (2007). Adaptations to energy stress dictate the ecology and evolution of the Archaea. Nat Rev Microbiol, 5(4): 316–323 https://doi.org/10.1038/nrmicro1619
48	Waldrop M P, Firestone M K (2006). Seasonal dynamics of microbial community composition and function in oak canopy and open grassland soils. Microb Ecol, 52(3): 470–479 https://doi.org/10.1007/s00248-006-9100-6
49	Wallenstein M D, Hall E K (2012). A trait-based framework for predicting when and where microbial adaptation to climate change will affect ecosystem functioning. Biogeochemistry, 109(1–3): 35–47 https://doi.org/10.1007/s10533-011-9641-8
50	Yao H, Gao Y, Nicol G W, Campbell C D, Prosser J I, Zhang L, Han W, Singh B K (2011). Links between ammonia oxidizer community structure, abundance, and nitrification potential in acidic soils. Appl Environ Microbiol, 77(13): 4618–4625 https://doi.org/10.1128/AEM.00136-11

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