Redox Fluctuations Frame Microbial Community Impacts on N-cycling Rates in a Humid Tropical Forest Soil
Tóm tắt
Fluctuating soil redox regimes may facilitate the co-occurrence of microbial nitrogen transformations with significantly different sensitivities to soil oxygen availability. In an upland humid tropical forest, we explored the impact of fluctuating redox regimes on gross nitrogen cycling rates and microbial community composition. Our results suggest that the rapidly fluctuating redox conditions that characterize these upland soils allow anoxic and oxic N processing to co-occur. Gross nitrogen mineralization was insensitive to soil redox fluctuations. In contrast, nitrifiers in this soil were directly affected by low redox periods, yet retained some activity even after 3–6 weeks of anoxia. Dissimilatory nitrate reduction to ammonium (DNRA) was less sensitive to oxygen exposure than expected, indicating that the organisms mediating this reductive process were also tolerant of unfavorable (oxic) conditions. Denitrification was a stronger sink for NO
3
−
in consistently anoxic soils than in variable redox soils. Microbial biomass and community composition were maintained with redox fluctuation, but biomass decreased and composition changed under static oxic and anoxic soil regimes. Bacterial community structure was significantly correlated with rates of nitrification, denitrification and DNRA, suggesting that redox-control of soil microbial community structure was an important determinant of soil N-cycling rates. Specific nitrogen cycling functional groups in this environment (such as nitrifiers, DNRA organisms, and denitrifiers) appear to have adapted to nutrient resources that are spatially and temporally variable. In soils where oxygen is frequently depleted and re-supplied, characteristics of microbial tolerance and resilience can frame N cycling patterns.
Tài liệu tham khảo
Ambus P, Mosier A, Christensen S (1992) Nitrogen turnover rates in a riparian fen determined by nitrogen-15 dilution. Bio Fert Soils 14:230–236
Armstrong RA (1976) Fugitive species: experiments with fungi and some theoretical considerations. Ecology 57:953–963
Bedard C, Knowles R (1989) Physiology biochemistry and specific inhibitors of methane ammonium ion and carbon monoxide oxidation by methanotrophs and nitrifiers. Microbiol Rev 53:68–84
Beinroth FH (1982) Some highly weathered soils of Puerto Rico, 1. Morphology, formation and classification. Geoderma 27:1–73
Bengtsson G, Bergwall C (2000) Fate of 15N labeled nitrate and ammonium in a fertilized forest soil. Soil Biol Biochem 32:545–557
Binnerup SJ, Jensen K, Revsbech NP, Jensen MH, Sorensen J (1992) Denitrification, dissimilatory reduction of nitrate to ammonium, and nitrification in a bioturbated estuarine sediment as measured with nitrogen-15 and microsensor techniques. App Environ Microbiol 58:303–313
Bodelier PLE, Libochant JA, Blom CWPM, Laanbroek HJ (1996) Dynamics of nitrification and denitrification in root-oxygenated sediments and adaptation of ammonia-oxidizing bacteria to low-oxygen or anoxic habitats. App Environ Microbiol 62:4100–4107
Bonin P (1996) Anaerobic nitrate reduction to ammonium in two strains isolated from coastal marine sediment—a dissimulatory pathway. FEMS Microbiol Ecol 19:27–38
Breuer L, Kiese R, Butterbach-Bahl K (2002) Temperature and moisture effects on nitrification rates in tropical rain-forest soils. Soil Sci Soc Am J 66:834–844
Brodie E, Edwards S, Clipson N (2002) Bacterial community dynamics across a floristic gradient in a temperate upland grassland ecosystem. Microb Ecol 44:260–270
Brooks PD, Herman DJ, Atkins GJ, Prosser SJ, Barrie A (1993) Rapid, isotopic analysis of selected soil gases at atmospheric concentrations. In: Harper LA, Mosier AR, Duxbury JM, Rolston DE (eds) Agricultural ecosystem effects on trace gases and global climate change. ASA special publication number 55, Amreican Society of Agronomy, Madison, WI, pp 193–202
Brown S, Lugo AE, Silander S, Liegel L (1983) Research history and opportunities in the Luquillo experimental forest Puerto-Rico. US Forest Serv Gen Tech Rep 44:1–128
Brunet RC, Garciagil LJ (1996) Sulfide-induced dissimilatory nitrate reduction to ammonia in anaerobic freshwater sediments. FEMS Microbiol Ecol 21:131–138
Buresh RJ, Patrick WHJ (1981) Nitrate reduction to ammonium and organic nitrogen in an estuarine sediment. Soil Biol Biochem 13:279–284
Carucci A, Lindrea K, Majone M, Ramadori R (1999) Different mechanisms for the anaerobic storage of organic substrates and their effect on enhanced biological phosphate removal (EBPR). Water Sci Tech 39:21–28
Caskey WH, Tiedje JM (1979) Evidence for clostridia as agents of dissimilatory reduction of nitrate to ammonium in soils. Soil Sci Soc Am J 43:931–936
Cole J (1996) Nitrate reduction to ammonia by enteric bacteria-redundancy, or a strategy for survival during oxygen starvation. FEMS Microbiol Lett 136:1–11
Corre MD, Besse FO, Brumme R (2003) Soil nitrogen cycle in high nitrogen deposition forest:changes under nitrogen saturation and liming. Ecol App 13:287–298
Dalsgaard T, Bak F (1994) Nitrate reduction in a sulfate-reducing bacterium, desulfovibrio desulfuricans, isolated from rice paddy soil: Sulfide inhibition, kinetics, and regulation. App Env Microbiol 60:291–297
Davidson EA, Hart SC, Shanks CA, Firestone MK (1991) Measuring gross nitrogen mineralization immobilization and nitrification by nitrogen-15 isotopic pool dilution in intact soil cores. J Soil Sci 42:335–350
Davidson EA, Swank WT, Perry TO (1986) Distinguishing between nitrification and denitrification as sources of gaseous nitrogen production in soil. App Env Microbiol 52:1280–1286
Eriksson PG, Svensson JM, Carrer GM (2003) Temporal changes and spatial variation of soil oxygen consumption, nitrification and denitrification rates in a tidal salt marsh of the lagoon of Venice, Italy. Estuar Coast Shelf Sci 58:861–871
Fenchel T, Finlay BJ (1995) Ecology and evolution in anoxic worlds. Oxford Univeristy Press, Oxford, UK
Fenchel T, King G, Blackburn TH (1998) Bacterial biogeochemistry: the ecophysiology of mineral cycling. Academic Press, San Diego
Firestone MK, Davidson EA (1989) Microbiological basis of NO and N2O production and consumption in soil. In: Andreae MO, Schimel DS (eds) Exchange of trace gases between terrestrial ecosystems and the atmosphere. John Wiley and Sons Ltd., New York, NY, pp 7–21
Hall GH, Jeffries C (1984) The contribution of nitrification in the water column and profundal sediments to the total oxygen deficit of the hypolimnion of a mesotrophic lake Grasmere english lake district UK. Microb Ecol 10:37–46
Hart SC, Stark JM, Davison EA, Firestone MK (1994) Nitrogen mineralization, immobilization and nitrification. In: Methods of soil analysis, Part II. Microbiological and biochemical properties. Soil Science Society of America, Madison, WI, pp 985–1017
Heins Y (1987) Survival and dormancy of microorganisms. John Wiley and Sons, New York, NY
Herman DJ, Brooks PD, Ashraf M, Azam F, Mulvaney RL (1995) Evaluation of methods for nitrogen-15 analysis of inorganic nitrogen in soil extracts. I. Diffusion methods. Commun Soil Sci Plant Anal 26:1675–1685
Hutchinson GE (1961) The paradox of the plankton. Amer Nat 95:137–145
Imlay JA (2002) How oxygen damages microbes: oxygen tolerance and obligate anaerobiosis. Adv Microb Physiol 41:111–153
Jensen K, Revsbech NP, Nielsen LP (1993) Microscale distribution of nitrification activity in sediment determined with a shielded microsensor for nitrate. App Environ Microbiol 59:3287–3296
Jorgensen KS (1989) Annual pattern of denitrification and nitrate ammonification in estuarine sediment. App Environ Microbiol 55:1841–1847
Keith-Roach MJ, Bryan ND, Bardgett RD, Livens FR (2002) Seasonal changes in the microbial community of a salt marsh, measured by phospholipid fatty acid analysis. Biogeochemistry 60:77–96
Kieft TL, Murphy EM, Haldeman DL, Amy PS, Bjornstad BN, McDonald EV, Ringelberg DB, White DC, Stair J, Gsell RP, Griffiths TC, Holben WE, Boone DR (1998) Microbial transport, survival, and succession in a sequence of buried sediments. Microb Ecol 36:336–348
King D, Nedwell DB (1985) The influence of nitrate concentration upon the end-products of nitrate dissimilation by bacteria in anaerobic salt marsh sediment. Microb Ecol 31:23–28
Lodge DJ, McDowell WH, McSwiney CP (1994) The importance of nutrient pulses in tropical forests. Trends Ecol Evolut 9:384–387
Matheson VG, MunakataMarr J, Hopkins GD, McCarty PL, Tiedje JM, Forney LJ (1997) A novel means to develop strain-specific DNA probes for detecting bacteria in the environment. App Env Microbiol 63:2863–2869
McGroddy M, Silver WL (2000) Variations in belowground carbon storage and soil CO2 flux rates along a wet tropical climate gradient. Biotropica 32:614–624
Murphy SF, Brantley SL, Blum AE, White AF, Dong H (1998) Chemical weathering in a tropical watershed, Luquillo mountains, Puerto Rico: I Rate and mechanism of biotite weathering. Geochim Cosmochim Acta 62:227–243
Myrold DD (1987) Relationship between microbial biomass nitrogen and a nitrogen availability index. Soil Sci Soc Am J 51:1047–1049
Myrold DD (2005) Microbial nitrogen transformations. In: Sylvia DM, Fuhrmann JJ, Hartel PG, Zuberer DA (eds) Principles and applications of soil microbiology, 2nd edn. Prentice Hall, Upper Saddle River, NJ, pp 333–372
Neill C, Piccolo MC, Melillo JM, Steudler PA, Cerri C (1999) Nitrogen dynamics in Amazon forest and pasture soils measured by 15N pool dilution. Soil Bio Biochem 31:567–572
Niviere V, Fontecave M (2004) Discovery of superoxide reductase: an historical perspective. J Biol Inorg Chem 9:119–123
Parkin TB (1990) Characterizing the variability of soil denitrification. In: Revsbech NP, Sorensen J (eds) Denitrification in soil and sediment. Plenum Press, New York, NY, pp 213–228
Peterson EB, McCune B (2001) Diversity and succession of epiphytic macrolichen communities in low-elevation managed conifer forests in western Oregon. J Veg Sci 12:511–524
Pett-Ridge J, Firestone M (2005) Redox fluctuation structures microbial community in a wet tropical soil. Appl Environ Microbiol 71:6998--7007
Philippot L, Hojberg O (1999) Dissimilatory nitrate reductases in bacteria. Biochim Biophys Acta 1446:1–23
Picek T, Simek M, Santruckova H (2000) Microbial responses to fluctuation of soil aeration status and redox conditions. Biol Fert Soil 31:315–322
Rudaz AO, Davidson EA, Firestone MK (1991) Sources of nitrous oxide production following wetting of dry soil. FEMS Microbiol Ecol 85:117–124
Satpathy SN, Rath AK, Ramakrishnan B, Rao VR, Adhya TK, Sethunathan N (1997) Diurnal variation in methane efflux at different growth stages of tropical rice. Plant Soil 195:267–271
Schimidt-Rohr K, Mao JD, Olk DC (2004) Nitrogen-bonded aromatics in soil organic matter and their implications for a yield decline in intensive rice cropping. SO—Proc Nat Acad Sci USA 101:6351–6354
Schuur EAG, Matson PA (2001) Net primary productivity and nutrient cycling across a mesic to wet precipitation gradient in Hawaiian montane forest. Oecologia 128:431–442
Silver WL, Herman DJ, Firestone MK (2001) Dissimilatory nitrate reduction to ammonium in upland tropical forest soils. Ecology 82:2410–2416
Silver WL, Lugo AE, Keller M (1999) Soil oxygen availability and biogeochemistry along rainfall and topographic gradients in upland wet tropical forest soils. Biogeochemistry 44:301–328
Silver WL, Thompson AW, Firestone MK, Reich A, Ewel JJ (2005) Nitrogen retention and loss in tropical plantation and old growth forests. Ecol App 15:1604–1614
Smith MS, Parsons LL (1985) Persistence of denitrifying enzyme activity in dried soils. App Environ Microbiol 49:316–320
Smorczewski WT, Schmidt EL (1991) Numbers, activities and diversity of autotrophic ammonia-oxidizing bacteria in a freshwater eutrophic lake sediment. Can J Microbiol 37:828–833
Sorensen J (1978) Capacity for denitrification and reduction of nitrate to ammonia in a coastal marine sediment. App Environ Microbiol 35:301–305
Stumm W, Morgan JJ (1981) Aquatic chemistry: an introduction emphasizing chemical equilibria in natural waters. John Wiley and Sons, New York, NY
Takaya N (2002) Dissimilatory nitrate reduction metabolisms and their control in fungi. J Biosci Bioengineer 94:506–510
Tiedje JM (1988) Ecology of denitrification and dissimilatory nitrate reduction to ammonium. In: Zehnder AJB (ed) Biology of Anaerobic Microorganisms. John Wiley and Sons, New York, NY, pp 178–244
Tiedje JM (1994) Denitrifiers. In: Methods of soil analysis, part II. Microbiological and biochemical properties. SSSA, Madison, WI
Tiedje JM, Sexstone AJ, Myrold DD, Robinson JA (1982) Denitrification: ecological niches, competition and survival. Antonie de Leeuwenhock 48:569–583
Tiedje JM, Sextone AJ, Parkin TB, Revsbech NP (1984) Anaerobic processes in soil. Plant Soil 76:197–212
Twining JR, Zaw M, Russell R, Wilde K (2004) Seasonal changes of redox potential and microbial activity in two agricultural soils of tropical Australia: Some implications for soil-to-plant transfer of radionuclides. J Environ Rad 76:265–272
Vanmiegroet H, Johnson DW, Cole DW (1990) Soil nitrification as affected by N-fertility and changes in forest floor C/N ratio in four forest soils. Can J Forest Res 20:1012–1019
Weaver PL (1994) Bano de Oro natural Area Luquillo mountains Puerto Rico. USDA Forest Service IITF, New Orleans, LA
Weinstein DA, Yanai RD (1994) Integrating the effect of simultaneous multiple stresses on plants using the simulation model TREGRO. J Env Qual 23:418–428
Wilkinson L (1990) Systat. The system for statistics. Systat, Inc., Evanston, IL
Zar JH (1996) Biostatistical analysis. Prentice-Hall, Inc., Upper Saddle River, NJ
Zhou Z, Takaya N, Nakamura A, Yamaguchi M, Takeo K, Shoun H (2002) Ammonia fermentation, a novel anoxic metabolism of nitrate by fungi. J Biol Chem 277:1892–1896