Soil- and enantiomer-specific metabolism of amino acids and their peptides by Antarctic soil microorganisms

Soil Biology and Biochemistry

Volumn 43, Issue 12, 2011, Pages 2410-2416

  Hill, Paul W ^a   Farrell, Mark ^a,b,c   Roberts, Paula ^a   Farrar, John ^a   Grant, Helen ^b   Newsham, Kevin K ^d   Hopkins, David W ^e   Bardgett, Richard D ^b   Jones, Davey L ^a  

^a BANGOR UNIVERSITY   (United Kingdom)

^b LANCASTER UNIVERSITY   (United Kingdom)

^c CSIRO   (Australia)

^d BRITISH ANTARCTIC SURVEY   (United Kingdom)

^e HERIOT WATT UNIVERSITY   (United Kingdom)

Author keywords

14C; Carbon cycling; Dissolved organic nitrogen; DON; Isomer; Mineralization; Oligopeptide; Permafrost

Indexed keywords

14C; CARBON CYCLING; DISSOLVED ORGANIC NITROGEN; DON; MINERALIZATION; OLIGOPEPTIDES;

AMINO ACIDS; CARBON DIOXIDE; CHIRALITY; ECOSYSTEMS; ENANTIOMERS; METABOLISM; MICROORGANISMS; MINERALOGY; MONOMERS; PEPTIDES; PERMAFROST;

SOILS;

AMINO ACID; DECOMPOSITION; DISSOLVED ORGANIC NITROGEN; GLOBAL WARMING; GRASS; LICHEN; LOW TEMPERATURE; METABOLISM; MINERALIZATION; PEPTIDE; PERMAFROST; PRIMARY PRODUCTION; PROTEIN; SOIL MICROORGANISM; SOIL ORGANIC MATTER; TERRESTRIAL ECOSYSTEM;

ANTARCTICA;

BACTERIA (MICROORGANISMS); BRYOPHYTA;

EID: 80052713254     PISSN: 00380717     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.soilbio.2011.08.006     Document Type: Article

References (58)

1. Amelung W. Nitrogen biomarkers and their fate in soil. Journal of Plant Nutrition & Soil Science 2003, 166:677-686.
2. Amelung W., Zhang X., Flach K.W. Amino acids in grassland soils: climatic effects on concentrations and chirality. Geoderma 2006, 130:207-217.
3. Björck S., Malmer N., Hjort C., Sandgren P., Ingólfsson Ó, Wallén B., Smith R.I.L., Jónsson B.L. Stratigraphic and paleoclimatic studies of a 5500-year-old moss bank on Elephant Island, Antarctica. Arctic and Alpine Research 1991, 23:361-374.
4. Boddy E.L., Roberts P., Hill P.W., Farrar J., Jones D.L. Turnover of low molecular weight dissolved organic C (DOC) and microbial C exhibit different temperature sensitivities in Arctic tundra soils. Soil Biology & Biochemistry 2008, 40:1557-1566.
5. Boulette M.L., Baynham P.J., Jorth P.A., Kukavica-Ibrulj I., Longoria A., Barrera K., Levesque R.C., Whiteley M. Characterization of alanine catabolism in Pseudomonas aeruginosa and its importance for proliferation in vivo. Journal of Bacteriology 2009, 191:6329-6334.
6. Brückner H., Westhauser T. Chromatographic determination of l- and d-amino acids in plants. Amino Acids 2003, 24:43-55.
7. Chapin F.S., Moilanen L., Kielland K. Preferential use of organic nitrogen for growth by a non-mycorrhizal arctic sedge. Nature 1993, 361:150-153.
8. Clegg C.D., Lovell R.D.L., Hobbs P.J. The impact of grassland management regime on the community structure of selected bacterial groups in soils. FEMS Microbiology Ecology 2003, 43:263-270.
9. D'Aniello A., D'Onofrio G., Pischetola M., D'Aniello G., Vetere A., Petrucelli L., Fisher G. Biological role of d-amino acid oxidase and d-aspartate oxidase. Effects of d-amino acids. Journal of Biological Chemistry 1993, 268:26941-26949.
10. Farrell M., Hill P.W., Farrar J.F., Bardgett R.D., Jones D.L. Seasonal variation in soluble soil carbon and nitrogen across a grassland productivity gradient. Soil Biology & Biochemistry 2011, 43:835-844.
11. Farrell M., Hill P.W., Wanniarachchi S.D., Farrar J.F., Bardgett R.D., Jones D.L. Rapid peptide metabolism: a major component of soil nitrogen cycling?. Global Biogeochemical Cycles 2011, GB3014.
12. Fenton J.H.C. The rate of peat accumulation in Antarctic moss banks. Journal of Ecology 1980, 68:211-228.
13. Friedman M. Chemistry, nutrition and microbiology of d-amino acids. Journal of Agricultural and Food Chemistry 1999, 47:3457-3479.
14. Gonzales T., Robert-Baudouy J. Bacterial aminopeptidases: properties and functions. FEMS Microbiology Reviews 1996, 18:319-344.
15. Hill P.W., Farrar J.F., Jones D.L. Decoupling of microbial glucose uptake and mineralization in soil. Soil Biology & Biochemistry 2008, 40:616-624.
16. Hill P.W., Farrar J., Roberts P., Farrell M., Grant H., Newsham K.K., Hopkins D.W., Bardgett R.D., Jones D.L. Vascular plant success in a warming Antarctic may be due to efficient nitrogen acquisition. Nature Climate Change 2011, 1:50-53.
17. Hill P.W., Quilliam R.S., DeLuca T.H., Farrar J.F., Farrell M., Roberts P., Newsham K.K., Hopkins D.W., Bardgett R.D., Jones D.L. Acquisition and assimilation of nitrogen as peptide-bound and D-enantiomers of amino acids by wheat. PLoS ONE 2011, 10.1371/journal.pone.0019220.
18. Hols P., Defrenne C., Ferain T., Derzelle S., Delplace B., Delcour J. The alanine racemase gene is essential for growth of Lactobacillus plantarum. Journal of Bacteriology 1997, 179:3804-3807.
19. Hopkins D.W., Ferguson K.E. Substrate induced respiration in soil amended with d- and l-isomers of amino acids. Applied Soil Ecology 1994, 1:75-81.
20. Hopkins D.W., O'Dowd R.W., Shiel R.S. Comparison of d- and l-amino acid metabolism in soils with differing microbial biomass and activity. Soil Biology & Biochemistry 1997, 29:23-29.
21. Jan M.T., Roberts P., Tonheim S.K., Jones D.L. Protein breakdown represents a major bottleneck in nitrogen cycling in grassland soils. Soil Biology & Biochemistry 2009, 41:2272-2282.
22. Janes B.K., Bender R.A. Alanine catabolism in Klebsiella aerogenes: molecular characterization of the dadAB operon and its regulation by the nitrogen assimilation control protein. Journal of Bacteriology 1998, 180:563-570.
23. Janoš P. Separation methods in the chemistry of humic substances. Journal of Chromatography A 2003, 983:1-18.
24. Jones D.L., Kielland K., Sinclair F.L., Dahlgren R.A., Newsham K.K., Farrar J.F., Murphy D.V. Soil organic nitrogen mineralization across a global latitudinal gradient. Global Biogeochemical Cycles 2009, 23:GB1016.
25. Jones D.L., Owen A.G., Farrar J.F. Simple method to enable the high resolution determination of total free amino acids in soil solutions and soil extracts. Soil Biology & Biochemistry 2002, 34:1893-1902.
26. Jørgensen N.O.G., Middelboe M. Occurrence and bacterial cycling of d amino acid isomers in an estuarine environment. Biogeochemistry 2006, 81:77-94.
27. Kimber R.W.L., Nannipieri P., Ceccanti B. The degree of racemization of amino acids released by hydrolysis of humic-protein complexes: implications for age assessment. Soil Biology & Biochemistry 1990, 22:181-185.
28. Komarova N.Y., Thor K., Gubler A., Meier S., Dietrich D., Weichert A., Suter-Grotemeyer M., Tegeder M., Rentsch D. AtPTR1 and AtPTR5 transport dipeptides in planta. Plant Physiology 2008, 148:856-869.
29. Kreil G. d-amino acids in animal peptides. Annual Review of Biochemistry 1997, 66:337-345.
30. Kullman J.P., Chen X., Armstrong D.W. Evaluation of the enantiomeric composition of amino acids in tobacco. Chirality 1999, 11:669-673.
31. Kuzyakov Y. Review: factors affecting rhizosphere priming effects. Journal of Plant Nutrition & Soil Science 2002, 165:382-396.
32. Leckie S.A. Methods of microbial community profiling and their application of forest soils. Forest Ecology & Management 2005, 220:88-106.
33. Lobocka M., Hennig J., Wild J., Kłopotowski T. Organization and expression of the Escherichia coli k-12 dad operon encoding the smaller subunit of d-amino acid dehydrogenase and the catabolic alanine racemase. Journal of Bacteriology 1994, 176:1500-1510.
34. Mahaney W.C., Rutter N.W. Amino acid d/l ratio distributions in two late quaternary soils in the afroalpine zone of Mount Kenya East Africa. Catena 1989, 16:205-214.
35. Manabe H. Formation of dipeptides containing d-alanine in wild rice plants. Phytochemistry 1992, 31:527-529.
36. Martínez-Rodríguez S., Martínez-Gómez A.I., Rodríguez-Vico F., Clemente-Jiménez J.M., Las Heras-Vásquez F.J. Natural occurrence and industrial applications of d-amino acids: an overview. Chemistry & Biodiversity 2010, 7:1531-1548.
37. Miller G.H., Magee J.W., Jull A.J.T. Low-latitude glacial cooling in the Southern Hemisphere from amino-acid racemization in emu eggshells. Nature 1997, 385:241-244.
38. Milligan D.L., Tran S.L., Strych U., Cook G.M., Krause K.L. The alanine racemase of Mycobacterium smegmatis is essential for growth in the absence of d-alanine. Journal of Bacteriology 2007, 189:8381-8386.
39. Miranda K.M., Espey M.G., Wink D.A. A rapid, simple, spectrophotometric method for simultaneous detection of nitrate and nitrite. Nitric Oxide 2001, 5:62-71.
40. Mulvaney R.L. Nitrogen-inorganic forms. Methods of Soil Analysis. Part 3. SSSA Book Ser. 5 1996, 1123-1184. Soil Science Society of America, Madison, WI. D.L. Sparks (Ed.).
41. Näsholm T., Kielland K., Ganeteg U. Uptake of organic nitrogen by plants. New Phytologist 2009, 182:31-48.
42. O'Dowd R.W., Barraclough D., Hopkins D.W. Nitrogen mineralization in soil amended with d- and l-leucine. Soil Biology & Biochemistry 1999, 31:1573-1578.
43. O'Dowd R.W., Hopkins D.W. Mineralization of carbon from d- and l-amino acids and d-glucose in two contrasting soils. Soil Biology & Biochemistry 1998, 30:2009-2016.
44. O'Dowd R.W., Parsons R., Hopkins D.W. Soil respiration induced by the d- and l-isomers of a range of amino acids. Soil Biology & Biochemistry 1997, 29:1665-1671.
45. 13C analysis of unique amino acids in the bacterial peptidoglycan cell wall. FEMS Microbiology Ecology 1998, 25:229-240.
46. Ping C.-L., Michaelson G.J., Jorgenson M.T., Kimble J.M., Epstein H., Romanovsky V.E., Walker D.A. High stocks of soil organic carbon in the North American Arctic region. Nature Geoscience 2008, 1:615-619.
47. Pollegioni L., Sacchi P.S., Pilone M.S., Molla G. Physiological functions of d-amino acid oxidases: from yeast to humans. Cellular and Molecular Life Sciences 2007, 64:1373-1394.
48. Quayle W.C., Peck L.S., Peat H., Ellis-Evans J.C., Harrigan P.R. Extreme responses to climate change in Antarctic lakes. Science 2002, 295:645.
49. Schimel J.P., Bennett J. Nitrogen mineralization: challenges of a changing paradigm. Ecology 2004, 85:591-602.
50. Smith R.I.L. Signy Island as a paradigm of biological and environmental change in Antarctic terrestrial ecosystems. Antarctic Ecosystems. Ecological Change and Conservation 1990, 32-50. Springer-Verlag, Berlin. K.R. Kerry, G. Hempel (Eds.).
51. Tonelli C. d-proline effect on l-proline-requiring mutants in Zea mays (L.). Plant Cell Physiology 1985, 26:1205-1210.
52. Trumbore S. Age of soil organic matter and soil respiration: radiocarbon constraints on belowground C dynamics. Ecological Applications 2000, 10:399-411.
53. Vaughan D.G., Marshall G.J., Connolley W.M., Parkinson C., Mulvaney R., Hodgson D.A., King J.C., Pudsey C.J., Turner J. Recent rapid regional climate warming on the Antarctic Peninsula. Climatic Change 2003, 60:243-274.
54. 15N incorporation into d-alanine: a new method for tracing nitrogen uptake by bacteria. Limnology and Oceanography: Methods 2005, 3:230-240.
55. Wasserman S.A., Daub E., Grisafi P., Botstein D., Walsh C.T. Calabolic alanine racemase from Salmonella typhimurium: DNA sequence, enzyme purification, and characterization. Biochemistry 1984, 23:5182-5187.
56. Weintraub M.N., Schimel J.P. Seasonal protein dynamics in Alaskan arctic tundra soils. Soil Biology & Biochemistry 2005, 37:1469-1475.
57. Wischern F., Lobe I., Amelung W., Müller T., Joergensen R.G., Buerkert A. Changes in amino acid enantiomers and microbial performance in soils from a subtropical mountain oasis in Oman abandoned for different periods. Biology & Fertility of Soils 2004, 39:398-406.
58. Wynn-Williams D.D. Comparative respirometry of peat decomposition on a latitudinal transect in the maritime Antarctic. Polar Biology 1984, 3:173-181.