The metagenome of the marine anammox bacterium ‘ Candidatus Scalindua profunda’ illustrates the versatility of this globally important nitrogen cycle bacterium

Abstract

Summary Anaerobic ammonium‐oxidizing (anammox) bacteria are responsible for a significant portion of the loss of fixed nitrogen from the oceans, making them important players in the global nitrogen cycle. To date, marine anammox bacteria found in marine water columns and sediments worldwide belong almost exclusively to the ‘ Candidatus Scalindua’ species, but the molecular basis of their metabolism and competitive fitness is presently unknown. We applied community sequencing of a marine anammox enrichment culture dominated by ‘ Candidatus Scalindua profunda’ to construct a genome assembly, which was subsequently used to analyse the most abundant gene transcripts and proteins. In the S. profunda assembly, 4756 genes were annotated, and only about half of them showed the highest identity to the only other anammox bacterium of which a metagenome assembly had been constructed so far, the freshwater ‘ Candidatus Kuenenia stuttgartiensis’. In total, 2016 genes of S. profunda could not be matched to the K. stuttgartiensis metagenome assembly at all, and a similar number of genes in K. stuttgartiensis could not be found in S. profunda . Most of these genes did not have a known function but 98 expressed genes could be attributed to oligopeptide transport, amino acid metabolism, use of organic acids and electron transport. On the basis of the S. profunda metagenome, and environmental metagenome data, we observed pronounced differences in the gene organization and expression of important anammox enzymes, such as hydrazine synthase (HzsAB), nitrite reductase (NirS) and inorganic nitrogen transport proteins. Adaptations of Scalindua to the substrate limitation of the ocean may include highly expressed ammonium, nitrite and oligopeptide transport systems and pathways for the transport, oxidation, and assimilation of small organic compounds that may allow a more versatile lifestyle contributing to the competitive fitness of Scalindua in the marine realm.

Shown for reading. Its publisher allows quoting it, not republishing it.

References 74

1. 1.

   Almeida CC, Romão CV, Lindley PF, Teixeira M, Saraiva LM. The role of the hybrid cluster protein in oxidative stress defense. J Biol Chem. 2006;281:32445-32450.

   Not in our library10.1074/jbc.m605888200

2. 2.

   An SM, Gardner WS. Dissimilatory nitrate reduction to ammonium (DNRA) as a nitrogen link, versus denitrification as a sink in a shallow estuary (Laguna Madre/Baffin Bay, Texas). Mar Ecol Prog Ser. 2002;237:41-50.

   Not in our library

3. 3.
   The RAST Server: Rapid Annotations using Subsystems Technology · 2008

   No notice
4. 4.

   Beliaev AS, Saffarini DA, McLaughlin JL, Hunnicutt D. MtrC, an outer membrane decahaem c cytochrome required for metal reduction in Shewanella putrefaciens MR-1. Mol Microbiol. 2001;39:722-730.

   Not in our library10.1046/j.1365-2958.2001.02257.x

5. 5.

   Bendtsen JD, Nielsen H, von Heijne G, Brunak S. Improved prediction of signal peptides: SignalP 3.0. J Mol Biol. 2004;340:783-795.

   Not in our library10.1016/j.jmb.2004.05.028

6. 6.

   Boyington JC, Gladyshev VN, Khangulov SV, Stadtman TC, Sun PD. Crystal structure of formate dehydrogenase H: catalysis involving Mo, molybdopterin, selenocysteine, and an Fe4S4 cluster. Science. 1997;275:1305-1308.

   Not in our library10.1126/science.275.5304.1305

7. 7.

   Braus-Stromeyer SA, Schnappauf G, Braus GH, Gossner AS, Drake HL. Carbonic anhydrase in Acetobacterium woodii and other acetogenic bacteria. J Bacteriol. 1997;179:7197-7200.

   Not in our library10.1128/jb.179.22.7197-7200.1997

8. 8.

   Broda E. Two kinds of lithotrophes missing in nature. Z Allg Mikrobiol. 1977;17:491-493.

   Not in our library10.1002/jobm.3630170611

9. 9.

   Campbell BJ, Smith JL, Hanson TE, Klotz MG, Stein LY, Lee CK, et al. Adaptations to submarine hydrothermal environments exemplified by the genome of Nautilia profundicola. PLoS Genet. 2009;5:1-19.

   Not in our library10.1371/journal.pgen.1000362

10. 10.

    Canfield DE, Glazer AN, Falkowski PG. The evolution and future of Earth's nitrogen cycle. Science. 2010;330:192-196.

    Not in our library10.1126/science.1186120

11. 11.

    Darling ACE, Mau B, Blattner FR, Perna NT. Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res. 2004;14:1394-1403.

    Not in our library10.1101/gr.2289704

12. 12.

    De Almeida NM, Maalcke WJ, Keltjens JT, Jetten MSM, Kartal B. Proteins and protein complexes involved in the biochemical reactions of anaerobic ammonium-oxidizing bacteria. Biochem Soc Trans. 2011;39:303-308.

    Not in our library10.1042/bst0390303

13. 13.

    Delcher AL, Harmon D, Kasif S, White O, Salzberg SL. Improved microbial gene identification with GLIMMER. Nucleic Acids Res. 1999;27:4636-4641.

    Not in our library10.1093/nar/27.23.4636

14. 14.

    DiChristina TJ, Moore CM, Haller CA. Dissimilatory Fe(III) and Mn(IV) reduction by Shewanella putrefaciens requires ferE, a homolog of the pulEgspE) type II protein secretion gene. J Bacteriol. 2002;184:142-151.

    Not in our library10.1128/jb.184.1.142-151.2002

15. 15.

    Do CB, Mahabhashyam MSP, Brudno M, Batzoglou S. ProbCons: probabilistic consistency-based multiple sequence alignment. Genome Res. 2005;15:330-340.

    Not in our library10.1101/gr.2821705

16. 16.

    Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32:1792-1797.

    Not in our library10.1093/nar/gkh340

17. 17.

    Fujii T, Sugino H, Rouse JD, Furukawa K. Characterization of the microbial community in an anaerobic ammonium-oxidizing biofilm cultured on a nonwoven biomass carrier. J Biosci Bioeng. 2002;94:412-418.

    Not in our library10.1016/s1389-1723(02)80218-3

18. 18.

    Füssel J, Lam P, Lavik G, Jensen MM, Holtappels M, Gunter M, Kuypers MMM. Nitrite oxidation in the Namibian oxygen minimum zone. ISME J. 2011.

    Not in our library10.1038/ismej.2011.178

19. 19.

    Gori F, Tringe SG, Kartal B, Machiori E, Jetten MSM. The metagenomic basis of anammox metabolism in Candidatus ‘Brocadia fulgida’. Biochem Soc Trans. 2011;39:1799-1804.

    Not in our library10.1042/bst20110707

20. 20.

    Hamersley MR, Lavik G, Woebken D, Rattray JE, Lam P, Hopmans EC, et al. Anaerobic ammonium oxidation in the Peruvian oxygen minimum zone. Limnol Oceanogr. 2007;52:923-933.

    Not in our library

21. 21.

    Heidelberg JF, Paulsen IT, Nelson KE, Gaidos EJ, Nelson WC, Read TD, et al. Genome sequence of the dissimilatory metal ion-reducing bacterium Shewanella oneidensis. Nat Biotechnol. 2002;20:1118-1123.

    Not in our library10.1038/nbt749

22. 22.

    Huson DH, Auch AF, Qi J, Schuster SC. MEGAN analysis of metagenomic data. Genome Res. 2007;17:377-386.

    Not in our library10.1101/gr.5969107

23. 23.

    Jensen MM, Lam P, Revsbech NP, Nagel B, Gaye B, Jetten MSM, Kuypers MMM. Intensive nitrogen loss over the Omani Shelf due to anammox coupled with dissimilatory nitrite reduction to ammonium. ISME J. 2011;5:1660-1670.

    Not in our library10.1038/ismej.2011.44

24. 24.

    Jetten MSM, van Niftrik L, Strous M, Kartal B, Keltjens JT, Op den Camp HJM. Biochemistry and molecular biology of anammox bacteria. Crit Rev Biochem Mol Biol. 2009;44:65-84.

    Not in our library10.1080/10409230902722783

25. 25.

    Jetten MSM, Op den Camp HJM, Kuenen JG, Strous M, Krieg NR, Staley JT, Hedlund BP, Paster BJ, Ward N, Ludwig W, Whitman WB. Description of the order Brocadiales. The Bacteroidetes, Spirochaetes, Tenericutes (Mollicutes), Acidobacteria, Fibrobacteres, Fusobacteria, Dictyoglomi, Gemmatimonadetes, Lentisphaerae, Verrucomicrobia, Chlamydiae, and Planctomycetes. 2010;506-603.

    Not in our library

26. 26.

    Kanehisa M. The KEGG database. In Silico Sim Biol Proc. 2002;247:91-103.

    Not in our library

27. 27.

    Kartal B, Kuypers MMM, Lavik G, Schalk J, Op den Camp HJM, Jetten MSM, Strous M. Anammox bacteria disguised as denitrifiers: nitrate reduction to dinitrogen gas via nitrite and ammonium. Environ Microbiol. 2007;9:635-642.

    Not in our library10.1111/j.1462-2920.2006.01183.x

28. 28.

    Kartal B, Kuenen JG, van Loosdrecht MCM. Sewage treatment with anammox. Science. 2010a;328:702-703.

    Not in our library10.1126/science.1185941

29. 29.

    Kartal B, Tan NCG, Van de Biezen E, Kampschreur MJ, Van Loosdrecht MCM, Jetten MSM. Effect of nitric oxide on anammox bacteria. Appl Environ Microbiol. 2010b;76:6304-6306.

    Not in our library10.1128/aem.00991-10

30. 30.

    Kartal B, Maalcke WJ, De Almeida NM, Cirpus I, Gloerich J, Geerts W, et al. Molecular mechanism of anaerobic ammonium oxidation: a major source of nitrogen for our atmosphere. Nature. 2011;479:127-130.

    Not in our library10.1038/nature10453

31. 31.

    Klotz MG, Stein LY. Nitrifier genomics and evolution of the nitrogen cycle. FEMS Microbiol Lett. 2008;278:146-156.

    Not in our library10.1111/j.1574-6968.2007.00970.x

32. 32.

    Klotz MG, Schmid MC, Strous M, Op Den Camp HJM, Jetten MSM, Hooper AB. Evolution of an octahaem cytochrome c protein family that is key to aerobic and anaerobic ammonia oxidation by bacteria. Environ Microbiol. 2008;10:3150-3163.

    Not in our library10.1111/j.1462-2920.2008.01733.x

33. 33.

    Kuypers MMM, Sliekers AO, Lavik G, Schmid M, Jorgensen BB, Kuenen JG, et al. Anaerobic ammonium oxidation by anammox bacteria in the Black Sea. Nature. 2003;422:608-611.

    Not in our library10.1038/nature01472

34. 34.

    Kuypers MMM, Lavik G, Woebken D, Schmid M, Fuchs BM, Amann R, et al. Massive nitrogen loss from the Benguela upwelling system through anaerobic ammonium oxidation. Proc Natl Acad Sci USA. 2005;102:6478-6483.

    Not in our library10.1073/pnas.0502088102

35. 35.

    Lam P, Kuypers MMM. Microbial nitrogen cycling processes in oxygen minimum zones. Annu Rev Marine Sci. 2011;3:317-345.

    Not in our library10.1146/annurev-marine-120709-142814

36. 36.

    Lam P, Jensen MM, Lavik G, McGinnis DF, Muller B, Schubert CJ, et al. Linking crenarchaeal and bacterial nitrification to anammox in the Black Sea. Proc Natl Acad Sci USA. 2007;104:7104-7109.

    Not in our library10.1073/pnas.0611081104

37. 37.

    Lam P, Lavik G, Jensen MM, van de Vossenberg J, Schmid M, Woebken D, et al. Revising the nitrogen cycle in the Peruvian oxygen minimum zone. Proc Natl Acad Sci USA. 2009;106:4752-4757.

    Not in our library10.1073/pnas.0812444106

38. 38.

    Lovley DR, Holmes DE, Nevin KP. Dissimilatory Fe(III) and Mn(IV) reduction. Adv Microb Physiol. 2004;49:219-286.

    Not in our library10.1016/s0065-2911(04)49005-5

39. 39.

    Lücker S, Wagner M, Maixner F, Pelletier E, Koch H, Vacherie B, et al. A Nitrospira metagenome illuminates the physiology and evolution of globally important nitrite-oxidizing bacteria. Proc Natl Acad Sci USA. 2010;107:13479-13484.

    Not in our library10.1073/pnas.1003860107

40. 40.

    Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar, et al. ARB: a software environment for sequence data. Nucleic Acids Res. 2004;32:1363-1371.

    Not in our library10.1093/nar/gkh293

41. 41.

    Maidak BL, Cole JR, Lilburn TG, Parker CT, Saxman PR, Stredwick JM, et al. The RDP (Ribosomal Database Project) continues. Nucleic Acids Res. 2000;28:173-174.

    Not in our library10.1093/nar/28.1.173

42. 42.
    The DOE-JGI Standard Operating Procedure for the Annotations of Microbial Genomes · 2009

    No notice
43. 43.
    A predicted physicochemically distinct sub-proteome associated with the intracellular organelle of the anammox bacterium <it>Kuenenia stuttgartiensis</it> · 2010

    Not checked
44. 44.

    Moir JWB, Wood NJ. Nitrate and nitrite transport in bacteria. Cell Mol Life Sci. 2001;58:215-224.

    Not in our library10.1007/pl00000849

45. 45.

    Mulder A, Van de Graaf AAV, Robertson LA, Kuenen JG. Anaerobic ammonium oxidationdiscovered in a denitrifying fluidized bed reactor. FEMS Microbiol Ecol. 1995;16:177-183.

    Not in our library

46. 46.

    van Niftrik L, van Helden M, Kirchen S, van Donselaar EG, Harhangi HR, Webb RI, et al. Intracellular localization of membrane-bound ATPases in the compartmentalized anammox bacterium ‘Candidatus Kuenenia stuttgartiensis’. Mol Microbiol. 2010;77:701-715.

    Not in our library10.1111/j.1365-2958.2010.07242.x

47. 47.

    Penton CR, Devol AH, Tiedje JM. Molecular evidence for the broad distribution of anaerobic ammonium-oxidizing bacteria in freshwater and marine sediments. Appl Environ Microbiol. 2006;72:6829-6832.

    Not in our library10.1128/aem.01254-06

48. 48.

    Pitcher A, Villanueva L, Hopmans EC, Schouten S, Reichart G-J, Sinninghe Damsté JS. Niche segregation of ammonia-oxidizing archaea and anammox bacteria in the Arabian Sea oxygen minimum zone. ISME J. 2011;5:1896-1904.

    Not in our library10.1038/ismej.2011.60

49. 49.

    Ragsdale SW. Life with carbon monoxide. Crit Rev Biochem Mol Biol. 2004;39:165-195.

    Not in our library10.1080/10409230490496577

50. 50.

    Rowe JJ, Ubbink-Kok T, Molenaar D, Konings WN, Driessen AJM. NarK is a nitrite-extrusion system involved in anaerobic nitrate respiration by Escherichia coli. Mol Microbiol. 1994;12:579-586.

    Not in our library10.1111/j.1365-2958.1994.tb01044.x

51. 51.

    Rutherford K, Parkhill J, Crook J, Horsnell T, Rice P, Rajandream MA, Barrell B. Artemis: sequence visualization and annotation. Bioinformatics. 2000;16:944-945.

    Not in our library10.1093/bioinformatics/16.10.944

52. 52.

    Saier MH, Eng BH, Fard S, Garg J, Haggerty DA, Hutchinson WJ, et al. Phylogenetic characterization of novel transport protein families revealed by genome analyses. Biochim Biophys Acta Rev Biomembr. 1999;1422:1-56.

    Not in our library10.1016/s0304-4157(98)00023-9

53. 53.

    Sakka K, Nakajima J, Sakka M, Kimura T, Furukawa K. Enrichment of anammox bacteria from marine environment for the construction of a bioremediation reactor. Appl Microbiol Biotechnol. 2008;77:1159-1166.

    Not in our library10.1007/s00253-007-1247-7

54. 54.

    Salzberg SL, Delcher AL, Kasif S, White O. Microbial gene identification using interpolated Markov models. Nucleic Acids Res. 1998;26:544-548.

    Not in our library10.1093/nar/26.2.544

55. 55.

    Schalk J, de Vries S, Kuenen JG, Jetten MSM. Involvement of a novel hydroxylamine oxidoreductase in anaerobic ammonium oxidation. Biochemistry. 2000;39:5405-5412.

    Not in our library10.1021/bi992721k

56. 56.

    Schmid MC, Maas B, Dapena A, van de Pas-Schoonen K, van de Vossenberg J, Kartal B, et al. Biomarkers for in situ detection of anaerobic ammonium-oxidizing (anammox) bacteria. Appl Environ Microbiol. 2005;71:1677-1684.

    Not in our library10.1128/aem.71.4.1677-1684.2005

57. 57.

    Schmid MC, Risgaard-Petersen N, Van de Vossenberg J, Kuypers MMM, Lavik G, Petersen J, et al. Anaerobic ammonium-oxidizing bacteria in marine environments: widespread occurrence but low diversity. Environ Microbiol. 2007;9:1476-1484.

    Not in our library10.1111/j.1462-2920.2007.01266.x

58. 58.

    Shimamura M, Nishiyama T, Shigetomo H, Toyomoto T, Kawahara Y, Furukawa K, Fujii T. Isolation of a multiheme protein with features of a hydrazine-oxidizing enzyme from an anaerobic ammonium-oxidizing enrichment culture. Appl Environ Microbiol. 2007;73:1065-1072.

    Not in our library10.1128/aem.01978-06

59. 59.

    Shimamura M, Nishiyama T, Shinya K, Kawahara Y, Furukawa K, Fujii T. Another multiheme protein, hydroxylamine oxidoreductase, abundantly produced in an anammox bacterium besides the hydrazine-oxidizing enzyme. J Biosci Bioeng. 2008;105:243-248.

    Not in our library10.1263/jbb.105.243

60. 60.

    Sonnhammer ELL, Von Heijne G, Krogh A, Glasgow J, Littlejohn T, Major F, Lathrop R, Sankoff D, Sensen C. A hidden Markov model for predicting transmembrane helices in protein sequences. Sixth International Conference on Intelligent Systems for Molecular Biology (ISMB-98). 1998;175-182.

    Not in our library

61. 61.

    Stewart FJ, Ulloa O, Delong EF. Microbial metatranscriptomics in a permanent marine oxygen minimum zone. Environ Microbiol. 2012;14:23-40.

    Not in our library10.1111/j.1462-2920.2010.02400.x

62. 62.

    Stramma L, Johnson GC, Sprintall J, Mohrholz V. Expanding oxygen-minimum zones in the tropical oceans. Science. 2008;320:655-658.

    Not in our library10.1126/science.1153847

63. 63.

    Strous M, Fuerst JA, Kramer EHM, Logemann S, Muyzer G, Van de Pas-Schoonen KT, et al. Missing lithotroph identified as new planctomycete. Nature. 1999;400:446-449.

    Not in our library10.1038/22749

64. 64.

    Strous M, Pelletier E, Mangenot S, Rattei T, Lehner A, Taylor MW, et al. Deciphering the evolution and metabolism of an anammox bacterium from a community genome. Nature. 2006;440:790-794.

    Not in our library10.1038/nature04647

65. 65.

    Tabita FR, Hanson TE, Li H, Satagopan S, Singh J, Chan S. Function, structure, and evolution of the RuBisCO-like proteins and their RuBisCO homologs. Microbiol Mol Biol Rev. 2007;71:576-599.

    Not in our library10.1128/mmbr.00015-07

66. 66.

    Thompson JD, Higgins DG, Gibson TJ. CLUSTAL-W– improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994;22:4673-4680.

    Not in our library10.1093/nar/22.22.4673

67. 67.

    van de Vossenberg J, Rattray JE, Geerts W, Kartal B, van Niftrik L, van Donselaar EG, et al. Enrichment and characterization of marine anammox bacteria associated with global nitrogen gas production. Environ Microbiol. 2008;10:3120-3129.

    Not in our library10.1111/j.1462-2920.2008.01643.x

68. 68.

    Waight AB, Love J, Wang DN. Structure and mechanism of a pentameric formate channel. Nat Struct Mol Biol. 2010;17:31-U45.

    Not in our library10.1038/nsmb.1740

69. 69.

    Wessels HJC, Gloerich J, der Biezen E, Jetten MSM, Kartal B. Liquid chromatography – mass spectrometry-based proteomics of Nitrosomonas. Methods Enzymol. 2011;486:465-482.

    Not in our library10.1016/b978-0-12-381294-0.00021-3

70. 70.

    Woebken D, Teeling H, Wecker P, Dumitriu A, Kostadinov I, DeLong EF, et al. Fosmids of novel marine Planctomycetes from the Namibian and Oregon coast upwelling systems and their cross-comparison with planctomycete genomes. ISME J. 2007;1:419-435.

    Not in our library10.1038/ismej.2007.63

71. 71.

    Woebken D, Lam P, Kuypers MMM, Naqvi SWA, Kartal B, Strous M, et al. A microdiversity study of anammox bacteria reveals a novel Candidatus Scalindua phylotype in marine oxygen minimum zones. Environ Microbiol. 2008;10:3106-3119.

    Not in our library10.1111/j.1462-2920.2008.01640.x

72. 72.

    Yan J, Op den Camp HJM, Jetten MSM, Hu YY, Haaijer SCM. Induced cooperation between marine nitrifiers and anaerobic ammonium-oxidizing bacteria by incremental exposure to oxygen. Syst Appl Microbiol. 2011;33:407-415.

    Not in our library10.1016/j.syapm.2010.08.003

73. 73.

    Yang B, Peng Y, Leung HCM, Yiu SM, Qin J, Li R, Chin FYL, Zhang A, Borodovsky M, Özsoyoglu G, Mikler AR. MetaCluster: unsupervised binningof environmental genomic fragments and taxonomic annotation. Proceedings of the First ACM International Conference on Bioinformatics and Computational Biology. 2010;170-179.

    Not in our library

74. 74.

    Zhou JZ, Bruns MA, Tiedje JM. DNA recovery from soils of diverse composition. Appl Environ Microbiol. 1996;62:316-322.

    Not in our library10.1128/aem.62.2.316-322.1996

Cited by papers we hold 1

• Nitric oxide-dependent anaerobic ammonium oxidation · 2019
  Corrected

Reads

A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.