DOI QR코드

DOI QR Code

Short-Term Effect of Elevated Temperature on the Abundance and Diversity of Bacterial and Archaeal amoA Genes in Antarctic Soils

  • Han, Jiwon (Department of Environmental Science and Ecological Engineering, Korea University) ;
  • Jung, Jaejoon (Department of Environmental Science and Ecological Engineering, Korea University) ;
  • Park, Minsuk (Department of Environmental Science and Ecological Engineering, Korea University) ;
  • Hyun, Seunghun (Department of Environmental Science and Ecological Engineering, Korea University) ;
  • Park, Woojun (Department of Environmental Science and Ecological Engineering, Korea University)
  • Received : 2013.05.08
  • Accepted : 2013.06.05
  • Published : 2013.09.28

Abstract

Global warming will have far-reaching effects on our ecosystem. However, its effects on Antarctic soils have been poorly explored. To assess the effects of warming on microbial abundance and community composition, we sampled Antarctic soils from the King George Island in the Antarctic Peninsula and incubated these soils at elevated temperatures of $5^{\circ}C$ and $8^{\circ}C$ for 14 days. The reduction in total organic carbon and increase in soil respiration were attributed to the increased proliferation of Bacteria, Fungi, and Archaea. Interestingly, bacterial ammonia monooxygenase (amoA) genes were predominant over archaeal amoA, unlike in many other environments reported previously. Phylogenetic analyses of bacterial and archaeal amoA communities via clone libraries revealed that the diversity of amoA genes in Antarctic ammonia-oxidizing prokaryotic communities were temperature-insensitive. Interestingly, our data also showed that the amoA of Antarctic ammonia-oxidizing bacteria (AOB) communities differed from previously described amoA sequences of cultured isolates and clone library sequences, suggesting the presence of novel Antarctic-specific AOB communities. Denitrification-related genes were significantly reduced under warming conditions, whereas the abundance of amoA and nifH increased. Barcoded pyrosequencing of the bacterial 16S rRNA gene revealed that Proteobacteria, Acidobacteria, and Actinobacteria were the major phyla in Antarctic soils and the effect of short-term warming on the bacterial community was not apparent.

Keywords

References

  1. Aislabie JM, Chhour KL, Saul DJ, Miyauchi S, Ayton J, Paetzold RF, et al. 2006. Dominant bacteria in soils of Marble Point and Wright Valley, Victoria Land, Antarctica. Soil Biol. Biochem. 38: 3041-3056. https://doi.org/10.1016/j.soilbio.2006.02.018
  2. Aislabie J, Jordan S, Barker GM. 2008. Relation between soil classification and bacterial diversity in soils of the Ross Sea region, Antarctica. Geoderma 144: 9-20. https://doi.org/10.1016/j.geoderma.2007.10.006
  3. Auguet JC, Barberan A, Casamayor EO. 2010. Global ecological patterns in uncultured Archaea. ISME J. 4: 182-190. https://doi.org/10.1038/ismej.2009.109
  4. Beman JM, Roberts KJ, Wegley L, Rohwer F, Francis CA. 2007. Distribution and diversity of archaeal ammonia monooxygenase genes associated with corals. Appl. Environ. Microbiol. 73: 5642-5647. https://doi.org/10.1128/AEM.00461-07
  5. Bernhard AE, Landry ZC, Blevins A, de la Torre JR, Giblin AE, Stahl DA. 2010. Abundance of ammonia-oxidizing archaea and bacteria along an estuarine salinity gradient in relation to potential nitrification rates. Appl. Environ. Microbiol. 76: 1285-1289. https://doi.org/10.1128/AEM.02018-09
  6. Bockheim JG, Tarnocai C. 1998. Recognition of cryoturbation for classifying permafrost-affected soils. Geoderma 81: 281-293. https://doi.org/10.1016/S0016-7061(97)00115-8
  7. Caffrey JM, Bano N, Kalanetra K, Hollibaugh JT. 2007. Ammonia oxidation and ammonia-oxidizing bacteria and archaea from estuaries with differing histories of hypoxia. ISME J. 1: 660-602. https://doi.org/10.1038/ismej.2007.79
  8. Cary SC, McDonald IR, Barrett JE, Cowan DA. 2010. On the rocks: the microbiology of Antarctic Dry Valley soils. Nat. Rev. Microbiol. 8: 129-138. https://doi.org/10.1038/nrmicro2281
  9. Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ, et al. 2009. The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res. 37: D141-D145. https://doi.org/10.1093/nar/gkn879
  10. Davidson EA, Janssens IA. 2006. Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440: 165-173. https://doi.org/10.1038/nature04514
  11. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, et al. 2006. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl. Environ. Microbiol. 72: 5069-5072. https://doi.org/10.1128/AEM.03006-05
  12. Freney JR, Trevitt ACF, de Datta SK, Obcemea WN, Real JG. 1990. The interdependence of ammonia volatilization and denitrification as nitrogen loss processes in flooded rice fields in the Philippines. Biol. Fertil. Soils 9: 31-36. https://doi.org/10.1007/BF00335858
  13. Friedmann EI, Kappen L, Meyer MA, Nienow JA. 1993. Long-term productivity in the cryptoendolithic microbial community of the Ross Desert, Antarctica. Microb. Ecol. 25: 51-69.
  14. Han J, Jung J, Hyun S, Park H, Park W. 2012. Effects of nutritional input and diesel contamination on soil enzyme activities and microbial communities in Antarctic soils. J. Microbiol. 50: 916-924. https://doi.org/10.1007/s12275-012-2636-x
  15. Hansel CM, Fendorf S, Jardine PM, Francis CA. 2008. Changes in bacterial and archaeal community structure and functional diversity along a geochemically variable soil profile. Appl. Environ. Microbiol. 74: 1620-1633. https://doi.org/10.1128/AEM.01787-07
  16. Hatzenpichler R, Lebedeva EV, Spieck E, Stoecker K, Richter A, Daims H, et al. 2008. A moderately thermophilic ammonia-oxidizing crenarchaeote from a hot spring. Proc. Natl. Acad. Sci. USA 105: 2134-2139. https://doi.org/10.1073/pnas.0708857105
  17. Jin T, Zhang T, Ye L, Lee OO, Wong YH, Qian PY. 2011. Diversity and quantity of ammonia-oxidizing Archaea and Bacteria in sediment of the Pearl River Estuary, China. Appl. Microbiol. Biotechnol 90: 1137-1145. https://doi.org/10.1007/s00253-011-3107-8
  18. Jung J, Yeom J, Kim J, Han J, Lim HS, Park H, et al. 2011. Change in gene abundance in the nitrogen biogeochemical cycle with temperature and nitrogen addition in Antarctic soils. Res. Microbiol. 162: 1018-1026. https://doi.org/10.1016/j.resmic.2011.07.007
  19. Jung J, Seo H, Lee SH, Jeon CO, Park W. 2013. The effect of toxic malachite green on the bacterial community in Antarctic soil and the physiology of malachite green-degrading Pseudomonas sp. MGO. Appl. Microbiol. Biotechnol. 97: 4511-4521. https://doi.org/10.1007/s00253-012-4669-9
  20. Jung J, Choi S, Jung H, Scow KM, Park W. 2013. Primers for amplification of nitrous oxide reductase genes associated with Firmicutes and Bacteroidetes in organic-compound-rich soils. Microbiology 159: 307-315. https://doi.org/10.1099/mic.0.060194-0
  21. Kayee P, Sonthiphand P, Rongsayamanont C, Limpiyakorn T. 2011. Archaeal amoA genes outnumber bacterial amoA genes in municipal wastewater treatment plants in Bangkok. Microb. Ecol. 62: 776-788. https://doi.org/10.1007/s00248-011-9893-9
  22. Koops HP, Pommerening-Roser A. 2001. Distribution and ecophysiology of the nitrifying bacteria emphasizing cultured species. FEMS Microbiol. Ecol. 37: 1-9. https://doi.org/10.1111/j.1574-6941.2001.tb00847.x
  23. Lam P, Jensen MM, Lavik G, McGinnis DF, Muller B, Schubert CJ, et al. 2007. Linking crenarchaeal and bacterial nitrification to anammox in the Black Sea. Proc. Natl. Acad. Sci. USA 104: 7104-7109. https://doi.org/10.1073/pnas.0611081104
  24. Leininger S, Urich T, Schloter M, Schwark L, Qi J, Nicol GW, et al. 2006. Archaea predominate among ammoniaoxidizing prokaryotes in soils. Nature 442: 806-809. https://doi.org/10.1038/nature04983
  25. Mincer TJ, Church MJ, Taylor LT, Preston C, Karl DM, DeLong EF. 2007. Quantitative distribution of presumptive archaeal and bacterial nitrifiers in Monterey Bay and the North Pacific Subtropical Gyre. Environ. Microbiol. 9: 1162-1175. https://doi.org/10.1111/j.1462-2920.2007.01239.x
  26. Mosier AC, Francis CA. 2008. Relative abundance and diversity of ammonia-oxidizing archaea and bacteria in the San Francisco Bay estuary. Environ. Microbiol. 10: 3002-3016. https://doi.org/10.1111/j.1462-2920.2008.01764.x
  27. Niederberger TD, McDonald IR, Hacker AL, Soo RM, Barrett JE, Wall DH, et al. 2008. Microbial community composition in soils of Northern Victoria Land, Antarctica. Environ. Microbiol. 10: 1713-1724. https://doi.org/10.1111/j.1462-2920.2008.01593.x
  28. Nicol GW, Leininger S, Schleper C, Prosser JI. 2008. The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxidizing archaea and bacteria. Environ. Microbiol. 10: 2966-2978. https://doi.org/10.1111/j.1462-2920.2008.01701.x
  29. Ochsenreiter T, Selezi D, Quaiser A, Bonch-Osmolovskaya L, Schleper C. 2003. Diversity and abundance of Crenarchaeota in terrestrial habitats studied by 16S RNA surveys and real time PCR. Environ. Microbiol. 5: 787-797. https://doi.org/10.1046/j.1462-2920.2003.00476.x
  30. Pester M, Rattei T, Flechl S, Grongroft A, Richter A, Overmann J, et al. 2012. amoA-based consensus phylogeny of ammonia-oxidizing archaea and deep sequencing of amoA genes from soils of four different geographic regions. Environ. Microbiol. 14: 525-539. https://doi.org/10.1111/j.1462-2920.2011.02666.x
  31. Poage MA, Barrettt JE, Virginia RA, Wall DH. 2008. The influence of soil geochemistry on nematode distribution, McMurdo Dry Valleys, Antarctica. Arct. Antarct. Alp. Res. 40: 119-128. https://doi.org/10.1657/1523-0430(06-051)[POAGE]2.0.CO;2
  32. Purkhold U, Pommerening-Roser A, Juretschko S, Schmid MC, Koops HP, Wagner M. 2000. Phylogeny of all recognized species of ammonia oxidizers based on comparative 16S rRNA and amoA sequence analysis: implications for molecular diversity surveys. Appl. Environ. Microbiol. 66: 5368-5382. https://doi.org/10.1128/AEM.66.12.5368-5382.2000
  33. Ravishankara AR, Daniel JS, Portmann RW. 2009. Nitrous oxide (N2O): the dominant ozone-depleting substance emitted in the 21st century. Science 326: 123-125. https://doi.org/10.1126/science.1176985
  34. Smith JJ, Tow LA, Stafford W, Cary C, Cowan DA. 2006. Bacterial diversity in three different Antarctic Cold Desert mineral soils. Microb. Ecol. 51: 413-421. https://doi.org/10.1007/s00248-006-9022-3
  35. Smith RC, Prezelin BB, Baker KS, Bidigare RR, Boucher NP, Coley T, et al. 1992. Ozone depletion: ultraviolet radiation and phytoplankton biology in Antarctic waters. Science 255: 952-959. https://doi.org/10.1126/science.1546292
  36. Smith RL, Ceazan ML, Brooks MH. 1994. Autotrophic, hydrogen-oxidizing, denitrifying bacteria in groundwater, potential agents for bioremediation of nitrate contamination. Appl. Environ. Microbiol. 60: 1949-1955.
  37. Steig EJ, Schneider DP, Rutherford SD, Mann ME, Comiso JC, Shindell DT. 2009. Warming of the Antarctic ice-sheet surface since the 1957 International Geophysical Year. Science 457: 459-462.
  38. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28: 2731-2739. https://doi.org/10.1093/molbev/msr121
  39. Tourna M, Freitag TE, Nicol GW, Prosser JI. 2008. Growth, activity and temperature responses of ammonia-oxidizing archaea and bacteria in soil microcosms. Environ. Microbiol. 10: 1357-1364. https://doi.org/10.1111/j.1462-2920.2007.01563.x
  40. Venter JC, Remington K, Heidelberg JF, Halpern AL, Rusch D, Eisen JA, et al. 2004. Environmental genome shotgun sequencing of the Sargasso Sea. Science 304: 66-74. https://doi.org/10.1126/science.1093857
  41. Walker JK, Egger KN, Henry GH. 2008. Long-term experimental warming alters nitrogen-cycling communities but site factors remain the primary drivers of community structure in high Arctic tundra soils. ISME J. 2: 982-995. https://doi.org/10.1038/ismej.2008.52
  42. Wang YF, Gu JD. 2012 Higher diversity of ammonia/ ammonium-oxidizing prokaryotes in constructed freshwater wetland than natural coastal marine wetland. Appl. Microbiol. Biotechnol. 97: 7015-7033.
  43. Wuchter C, Abbas B, Coolen MJ, Herfort L, van Bleijswijk J, Timmers P, et al. 2006. Archaeal nitrification in the ocean. Proc. Natl. Acad. Sci. USA 103: 12317-12322. https://doi.org/10.1073/pnas.0600756103
  44. Yergeau E, Newsham KK, Pearce DA, Kowalchuk GA. 2007. Patterns of bacterial diversity across a range of Antarctic terrestrial habitats. Environ. Microbiol. 9: 2670-2682. https://doi.org/10.1111/j.1462-2920.2007.01379.x
  45. Zhang LM, Offre PR, He JZ, Verhamme DT, Nicol GW, Prosser JI. 2010. Autotrophic ammonia oxidation by soil thaumarchaea. Proc. Natl. Acad. Sci. USA 5: 17240-17245.

Cited by

  1. Influence of soil properties on archaeal diversity and distribution in the McMurdo Dry Valleys, Antarctica vol.89, pp.2, 2013, https://doi.org/10.1111/1574-6941.12322
  2. Metagenomics: Retrospect and Prospects in High Throughput Age vol.2015, pp.None, 2013, https://doi.org/10.1155/2015/121735
  3. Shifts in microbial trophic strategy explain different temperature sensitivity of CO2 flux under constant and diurnally varying temperature regimes vol.93, pp.5, 2013, https://doi.org/10.1093/femsec/fix063
  4. Effect of temperature on bacterial community in petroleum hydrocarbon-contaminated and uncontaminated Antarctic soil vol.41, pp.9, 2013, https://doi.org/10.1007/s00300-018-2316-3
  5. Short-Term Response of the Soil Microbial Abundances and Enzyme Activities to Experimental Warming in a Boreal Peatland in Northeast China vol.11, pp.3, 2013, https://doi.org/10.3390/su11030590
  6. Effects of Sea Animal Activities on Tundra Soil Denitrification and nirS‐ and nirK-Encoding Denitrifier Community in Maritime Antarctica vol.11, pp.None, 2013, https://doi.org/10.3389/fmicb.2020.573302
  7. Ammonia Oxidation Potentials and Ammonia Oxidizers of Lichen–Moss Vegetated Soils at Two Ice-free Areas in East Antarctica vol.35, pp.1, 2013, https://doi.org/10.1264/jsme2.me19126