Emission of nitrous oxide and dinitrogen by diverse earthworm families from Brazil and resolution of associated denitrifying and nitrate-dissimilating taxa

FEMS Microbiology Ecology

Volumn 83, Issue 2, 2013, Pages 375-391

  Depkat Jakob, Peter S ^a   Brown, George G ^b   Tsai, Siu M ^c   Horn, Marcus A ^a   Drake, Harold L ^a  

^a UNIVERSITY OF BAYREUTH   (Germany)

^b EMBRAPA CERRADOS   (Brazil)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Denitrification; Gut community; Invertebrate microbiology; Molecular microbial ecology; Soil microbiology

Indexed keywords

NITRATE; NITRATE REDUCTASE; NITROGEN; NITROUS OXIDE; NITROUS OXIDE REDUCTASE; OXIDOREDUCTASE;

BIOGENIC EMISSION; DENITRIFICATION; DOMINANCE; EARTHWORM; EMISSION INVENTORY; GENE EXPRESSION; MICROBIAL ACTIVITY; MICROBIAL ECOLOGY; NITROGEN; NITROUS OXIDE; SOIL MICROORGANISM; STOMACH CONTENT;

ANIMAL; ARTICLE; BACTERIUM; BRAZIL; CHEMISTRY; CLASSIFICATION; DENITRIFICATION; GASTROINTESTINAL TRACT; GENETICS; METABOLISM; MICROBIOLOGY; OLIGOCHAETA; SOIL;

ANIMALS; BACTERIA; BRAZIL; DENITRIFICATION; GASTROINTESTINAL TRACT; NITRATE REDUCTASE; NITRATES; NITROGEN; NITROUS OXIDE; OLIGOCHAETA; OXIDOREDUCTASES; SOIL; SOIL MICROBIOLOGY;

BRAZIL;

ACANTHODRILIDAE; AMYNTHAS; AMYNTHAS GRACILIS; DICHOGASTER; EUDRILIDAE; EUDRILUS; GLOSSOSCOLECIDAE; GLOSSOSCOLEX; INVERTEBRATA; LUMBRICIDAE; MEGASCOLECIDAE; PERIONYX; PONTOSCOLEX; RHINODRILUS; RHIZOBIALES;

EID: 84871991929     PISSN: 01686496     EISSN: 15746941     Source Type: Journal    
DOI: 10.1111/j.1574-6941.2012.01476.x     Document Type: Article

References (79)

1. Aira M, Monroy F & Dominguez J (2009) Changes in bacterial numbers and microbial activity of pig slurry during transit of epigeic and anecic earthworms. J Hazard Mater 162: 1404-1407.
2. Altschul SF, Gish W, Miller W, Myers EW & Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
3. Barois I & Lavelle P (1986) Changes in respiration rate and some physiochemical properties of a tropical soil during transit through Pontoscolex corethrurus (Glossoscolecidae, Oligochaeta). Soil Biol Biochem 18: 539-541.
4. Barois I, Brossard M, Lavelle P et al. (1999) Ecology of earthworm species with large environmental tolerance and/or extended distributions. Earthworm Management in Tropical Agroecosystems (Lavelle P, Hendrix P & Brussard L, eds), pp. 57-86. CAB International, London, UK.
5. 2O emissions in ploughed grassland? Soil Biol Biochem 39: 632-640.
6. Blakemore RJ (2000) Cosmopolitan Earthworms - An Eco-Taxonomic Guide to the Peregrine Species of the World. VermEcology, Kippax, Australia.
7. Borken W, Grundel S & Beese F (2000) Potential contribution of Lumbricus terrestris L. to carbon dioxide, methane, and nitrous oxide fluxes from a forest soil. Biol Fertil Soils 32: 142-148.
8. Bouché MB (1977) Strategies lombriciennes. Soil Organisms as Components of Ecosystems, Vol. 25 (Lohm U & Persson T, eds), pp. 122-132. Ecological Bulletins, Stockholm, Sweden.
9. Brown GG & Doube BM (2004) Functional interactions between earthworms, microorganisms, organic matter, and plants. Earthworm Ecology, 3rd edn (Edwards CA, ed), pp. 213-239. CRC Press, Boca Raton, FL.
10. Byzov BA, Nechtitaylo TY, Bumazhkin BK, Kurakov AV, Golyshin PN & Zvyagintsev DG (2009) Culturable microorganisms from the earthworm digestive tract. Mikrobiologiya 78: 360-368.
11. Casella S, Shapleigh JP & Payne WJ (1986) Nitrite reduction in Rhizobium "hedysari" strain HCNT 1. Arch Microbiol 146: 233-238.
12. Darwin C (1881) The Formation of Vegetable Mould Through the Action of Worms, With Observations of Their Habits. Murray, London, UK.
13. Depkat-Jakob PS, Hilgarth M, Horn MA & Drake HL (2010) Effect of earthworm feeding guilds on ingested dissimilatory nitrate reducers and denitrifiers in the alimentary canal of the earthworm. Appl Environ Microbiol 76: 6205-6214.
14. Depkat-Jakob PS, Hunger S, Schulz K, Brown GG, Tsai SM & Drake HL (2012) Emission of methane by Eudrilus eugeniae and other earthworms from Brazil. Appl Environ Microbiol 78: 3014-3019.
15. Drake HL & Horn MA (2006) Earthworms as a transient heaven for terrestrial denitrifying microbes: a review. Eng Life Sci 6: 261-265.
16. Drake HL & Horn MA (2007) As the worm turns: the earthworm gut as a transient habitat for soil microbial biomes. Annu Rev Microbiol 61: 169-189.
17. Egert M, Marhan S, Wagner B, Scheu S & Friedrich MW (2004) Molecular profiling of 16S rRNA genes reveals diet-related differences of microbial communities in soil, gut, and casts of Lumbricus terrestris L. (Oligochaeta: Lumbricidae). FEMS Microbiol Ecol 48: 187-197.
18. Enwall K, Philippot L & Hallin S (2005) Activity and composition of the denitrifying bacterial community respond differently to long-term fertilization. Appl Environ Microbiol 71: 8335-8343.
19. Falk S, Liu B & Braker G (2010) Isolation, genetic and functional characterization of novel soil nirK-type denitrifiers. Syst Appl Microbiol 33: 337-347.
20. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39: 783-791.
21. Furlong MA, Singleton DR, Coleman DC & Whitman WB (2002) Molecular and culture-based analyses of prokaryotic communities from an agricultural soil and the burrows and casts of the earthworm Lumbricus rubellus. Appl Environ Microbiol 68: 1265-1279.
22. Griffiths RI, Whiteley AS, O'Donnell AG & Bailey MJ (2000) Rapid method for coextraction of DNA and RNA from natural environments for analysis of ribosomal DNA and rRNA-based microbial community composition. Appl Environ Microbiol 66: 5488-5491.
23. Hallin S & Lindgren PE (1999) PCR detection of genes encoding nitrite reductase in denitrifying bacteria. Appl Environ Microbiol 65: 1652-1657.
24. Hamady M, Lozupone C & Knight R (2010) Fast UniFrac: facilitating high-throughput phylogenetic analyses of microbial communities including analysis of pyrosequencing and PhyloChip data. ISME J 4: 17-27.
25. Heisterkamp IM, Schramm A, de Beer D & Stief P (2010) Nitrous oxide production associated with coastal marine invertebrates. Mar Ecol Prog Ser 415: 1-9.
26. Henry S, Bru D, Stres B, Hallet S & Philippot L (2006) Quantitative detection of the nosZ gene, encoding nitrous oxide reductase, and comparison of the abundances of 16S rRNA, narG, nirK, and nosZ genes in soils. Appl Environ Microbiol 72: 5181-5189.
27. Heylen K, Vanparys B, Wittebolle L, Verstraete W, Boon N & de Vos P (2006) Cultivation of denitrifying bacteria: optimization of isolation conditions and diversity study. Appl Environ Microbiol 72: 2637-2643.
28. Hill TCJ, Walsh KA, Harris JA & Moffett BF (2003) Using ecological diversity measures with bacterial communities. FEMS Microbiol Ecol 43: 1-11.
29. 2O-producing microorganisms. Appl Environ Microbiol 69: 1662-1669.
30. Horn MA, Drake HL & Schramm A (2006a) Nitrous oxide reductase genes (nosZ) of denitrifying microbial populations in soil and the earthworm gut are phylogenetically similar. Appl Environ Microbiol 72: 1019-1026.
31. Horn MA, Mertel R, Kästner M, Gehre M & Drake HL (2006b) In vivo emission of dinitrogen by earthworms via denitrifying bacteria in the gut. Appl Environ Microbiol 72: 1013-1018.
32. Huse SM, Welch DM, Morrison HG & Sogin ML (2010) Ironing out the wrinkles in the rare biosphere through improved OUT clustering. Environ Microbiol 12: 1889-1898.
33. 2O-producing microorganisms in the gut of the earthworm Aporrectodea caliginosa are indicative of ingested soil bacteria. Appl Environ Microbiol 69: 1655-1661.
34. James SW & Brown GG (2006) Earthworm ecology and diversity in Brazil. Soil Biodiversity in Amazonian and Other Brazilian Ecosystems (Moreira FMS, Siqueira JO & Brussaard L, eds), pp. 56-116. CAB International, Wallingford, UK.
35. James SW & Guimarães A (2010) Discovery and development of new species for vermiculture. Vermiculture Technology: Earthworms, Organic Wastes and Environmental Management (Edwards CA, Arancon NQ & Sherman RL, eds), pp. 41-52. CRC Press, Boca Raton, FL.
36. Karsten GR & Drake HL (1995) Comparative assessment of the aerobic and anaerobic microfloras of earthworm guts and forest soils. Appl Environ Microbiol 61: 1039-1044.
37. 2O) by earthworms. Appl Environ Microbiol 63: 1878-1882.
38. Knapp BA, Podmirseg SM, Seeber J, Meyer E & Insam H (2009) Diet-related composition of gut microbiota of Lumbricus rubellus as revealed by a molecular fingerprinting technique and cloning. Soil Biol Biochem 41: 2299-2307.
39. Krištůfek V, Ravasz K & Pizl V (1992) Changes in densities of bacteria and microfungi during gut transit in Lumbricus rubellus and Aporrectodea caliginosa (Oligochaeta, Lumbricidae). Soil Biol Biochem 24: 1499-1500.
40. Kumar S, Nei M, Dudley J & Tamura K (2008) MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief Bioinform 9: 299-306.
41. Kunin V, Engelbrektson A, Ochman H & Hugenholz P (2010) Wrinkles in the rare biosphere: pyrosequencing errors can lead to artificial inflation of diversity estimates. Environ Microbiol 12: 118-123.
42. Lane DJ (1991) 16S/23S rRNA sequencing. Nucleic Acid Techniques in Bacterial Systematics (Stackebrandt E & Goodfellow M, eds), pp. 115-175. John Wiley and Sons, New York, NY.
43. Lee KE (1985) Earthworms. Their Ecology and Relationships With Soil and Land Use. Academic Press, Sydney, Australia.
44. Lozupone C & Knight R (2005) UniFrac a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71: 8228-8235.
45. 2O emission and crop-N uptake. Eur J Soil Sci 62: 152-161.
46. Makeschin F (1997) Earthworms (Lumbricidae: Oligochaeta): important promoters of soil development and soil fertility. Fauna in Soil Ecosystems (Benckiser G, ed), pp. 173-223. Marcel Dekker Inc., New York, NY.
47. 2O) by earthworms obtained from garden and forest soils. Appl Environ Microbiol 65: 3599-3604.
48. Nebel ME, Wild S, Holzhauser M, Hüttenberger L, Reitzig R, Sperber M, Wild S & Stoeck T (2011) Jaguc - a software package for environmental diversity analyses. J Bioinform Comput Biol 9: 749-773.
49. Palmer K, Drake HL & Horn MA (2009) Genome-derived criteria for assigning environmental narG and nosZ sequences to operational taxonomic units of nitrate reducers. Appl Environ Microbiol 75: 5170-5174.
50. 2O emission patterns from acidic soils in arctic tundra. ISME J 6: 1058-1077.
51. Philippot L, Piutti S, Martin-Laurent F, Hallet S & Germon JC (2002) Molecular analysis of the nitrate-reducing community from unplanted and maize-planted soils. Appl Environ Microbiol 68: 6121-6218.
52. Purkhold U, Pommerening-Roser A, Juretschko S, Schmidt 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 668: 5368-5382.
53. Quince C, Lanzen A, Curtis TP, Davenport RJ, Hall N, Head IM, Read LF & Sloan WT (2009) Accurate determination of microbial diversity from 454 pyrosequencing data. Nat Methods 6: 639-641.
54. 2O): the dominant ozone-depleting substance emitted in the 21st century. Science 326: 123-125.
55. Rich JJ, Heichen RS, Bottomley JP, Cromack K & Myrold DD (2003) Community composition and functioning of denitrifying bacteria from adjacent meadow and forest soils. Appl Environ Microbiol 69: 5974-5982.
56. Righi G (1971) Sobre a Familia Glossoscolecidae (Oligochaeta) no Brasil. Arq. Zool 20: 1-96.
57. Righi G (1990) Minhocas de Mato Grosso e de Rondônia. Programa Polonoroeste, Relatório de Pesquisa n 12. SCT/PR-CNPq, Programa do Trópico Úmido, Brasília, Brazil.
58. 2O emission from crop residue. Soil Biol Biochem 39: 2058-2069.
59. Saitou N & Nei M (1987) The neighbor-joining method - a new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406-425.
60. Schmidt O, Wüst PK, Hellmuth S, Borst K, Horn MA & Drake HL (2011) Novel [NiFe]- and [FeFe]-hydrogenase gene transcripts indicative of active facultative aerobes and obligate anaerobes in earthworm gut contents. Appl Environ Microbiol 77: 5842-5850.
61. Schönholzer F, Hahn D & Zeyer J (1999) Origins and fate of fungi and bacteria in the gut of Lumbricus terrestris L. studied by image analysis. FEMS Microbiol Ecol 28: 235-248.
62. Schönholzer F, Hahn D, Zarda B & Zeyer J (2002) Automated image analysis and in situ hybridization as tools to study bacterial populations in food resources, gut and cast of Lumbricus terrestris L. J Microbiol Methods 48: 53-68.
63. Singleton DR, Hendrix PF, Coleman DC & Whitman WB (2003) Identification of uncultured bacteria tightly associated with the intestine of the earthworm Lumbricus rubellus (Lumbricidae; Oligochaeta). Soil Biol Biochem 35: 1547-1555.
64. Smith SM (1983) Nitrous oxide production by Escherichia coli is correlated with nitrate reductase activity. Appl Environ Microbiol 45: 1545-1555.
65. Springett JA & Gray RAJ (1998) Burrowing behavior of the New Zealand indigenous earthworm Octochaetus multiporus (Megascolecidae: Oligochaeta). N Z J Ecol 22: 95-97.
66. Stackebrandt E & Ebers J (2006) Taxonomic parameters revisited: tarnished gold standards. Microbiol Today 33: 152-155.
67. Stief P & Schramm A (2010) Regulation of nitrous oxide emission associated with benthic invertebrates. Freshw Biol 55: 1647-1657.
68. Stief P, Poulsen M, Nielsen LP, Brix H & Schramm A (2009) Nitrous oxide emission by aquatic macrofauna. P Natl Acad Sci USA 106: 4296-4300.
69. Stolz JF & Basu P (2002) Evolution of nitrate reductase: molecular and structural variations on a common function. ChemBioChem 3: 198-206.
70. Stres B, Mahne I, Avgustin G & Tiedje MJ (2004) Nitrous oxide reductase (nosZ) gene fragments differ between native and cultivated Michigan soils. Appl Environ Microbiol 70: 301-309.
71. Sun YJ, Cai YP, Liu L, Yu FH, Farrell ML, McKendree W & Farmerie W (2009) ESPRIT: estimating species richness using large collections of 16S rRNA pyrosequences. Nucleic Acids Res 37: e76.
72. Thakuria D, Schmidt O, Finan D, Egan D & Doohan FM (2010) Gut wall bacteria of earthworms: a natural selection process. ISME J 4: 357-366.
73. Toffanin A, Wu QG, Maskus M, Casella S, Abruna HD & Shapleigh JP (1996) Characterization of the gene encoding nitrite reductase and the physiological consequences of its expression in the nondenitrifying Rhizobium "hedsari" strain HCNT1. Appl Environ Microbiol 62: 4019-4025.
74. Vine CE & Cole JA (2011) Unresolved sources, sinks, and pathways for the recovery of enteric bacteria from nitrosative stress. FEMS Microbiol Lett 325: 99-107.
75. Wolter C & Scheu S (1999) Changes in bacterial numbers and hyphal length during the gut passage through Lumbricus terrestris (Lumbricidae, Oligochaeta). Pedobiologia 43: 891-900.
76. Wüst PK, Horn MA & Drake HL (2009a) In situ hydrogen and nitrous oxide as indicators of concomitant fermentation and denitrification in the alimentary canal of the earthworm Lumbricus terrestris. Appl Environ Microbiol 75: 1852-1859.
77. Wüst PK, Horn MA, Henderson G, Janssen PH, Rehm BH & Drake HL (2009b) Gut-associated denitrification and in vivo emission of nitrous oxide by the earthworm families Megascolecidae and Lumbricidae in New Zealand. Appl Environ Microbiol 75: 3430-3436.
78. Yoshinari T & Knowles R (1976) Acetylene inhibition of nitrous oxide reduction by denitrifying bacteria. Biochem Biophys Res Commun 69: 705-710.
79. Zumft WG (1997) Cell biology and molecular basis of denitrification. Microbiol Mol Biol Rev 61: 533-616.