Metabolic network analysis reveals microbial community interactions in anammox granules

Nature Communications

Volumn 8, Issue , 2017, Pages

  Lawson, Christopher E ^a   Wu, Sha ^b   Bhattacharjee, Ananda S ^b   Hamilton, Joshua J ^c   McMahon, Katherine D ^a,c   Goel, Ramesh ^b   Noguera, Daniel R ^a,c  

^a University of Wisconsin Madison   (United States)

^b Department of Electrical and Computer Engineering   (United States)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETIC ACID; AMINO ACID TRANSPORTER; FORMIC ACID; NITRATE; NITRITE; AMMONIUM DERIVATIVE; NITRIC ACID DERIVATIVE; NITROGEN;

AMMONIUM; BACTERIUM; ECOSYSTEM FUNCTION; FUNCTIONAL ROLE; GENE EXPRESSION; METABOLISM; MICROBIAL COMMUNITY; NETWORK ANALYSIS; OXIDATION; POLLUTANT REMOVAL; WASTEWATER;

ANAMMOX BACTERIUM; ARTICLE; AUXOTROPHY; BACTERIAL GENE; BACTERIAL METABOLISM; CARBON METABOLISM; CATABOLISM; CHLOROBI; DENITRIFICATION; DETRITUS; ENERGY METABOLISM; EXTRACELLULAR SPACE; GENE EXPRESSION; HETEROTROPH; METABOLISM; METAGENOMICS; MICROBIAL COMMUNITY; NONHUMAN; PROTEIN DEGRADATION; TRANSCRIPTOMICS; BACTERIAL GENOME; BACTERIUM; BIOREACTOR; CHEMISTRY; GENETICS; HETEROTROPHY; MICROBIOLOGY; ORGANISMAL INTERACTION; OXIDATION REDUCTION REACTION; PHYSIOLOGY; PROCEDURES; TOXICITY; WASTE WATER; WATER MANAGEMENT;

CHLOROBI;

AMMONIUM COMPOUNDS; BACTERIA; BIOREACTORS; DENITRIFICATION; GENOME, BACTERIAL; HETEROTROPHIC PROCESSES; METABOLIC NETWORKS AND PATHWAYS; METAGENOMICS; MICROBIAL INTERACTIONS; NITRATES; NITRITES; NITROGEN; OXIDATION-REDUCTION; WASTE WATER; WATER PURIFICATION;

EID: 85020025763     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms15416     Document Type: Article

References (70)

1. Kartal, B., Kuenen, J. G. & van Loosdrecht, M. C. M. Sewage treatment with anammox. Science 328, 702-703 (2010).
2. Sliekers, A. O. et al. Completely autotrophic nitrogen removal over nitrite in one single reactor. Water Res. 36, 2475-2482 (2002).
3. Van Dongen, U., Jetten, M. S. M. & Van Loosdrecht, M. C. M. The SHARONAnammox process for treatment of ammonium rich wastewater. Water Sci. Technol. 44, 153-160 (2001).
4. Strous, M. et al. Deciphering the evolution and metabolism of an anammox bacterium from a community genome. Nature 440, 790-794 (2006).
5. Kartal, B. et al. Molecular mechanism of anaerobic ammonium oxidation. Nature 479, 127-130 (2011).
6. Kartal, B. et al. How to make a living from anaerobic ammonium oxidation. FEMS Microbiol. Rev. 37, 428-461 (2013).
7. Strous, M. et al. Missing lithotroph identified as new planctomycete. Nature 400, 446-449 (1999).
8. Abma, W. R. et al. Full-scale granular sludge Anammox process. Water Sci. Technol. 55, 27-33 (2007).
9. Ni, B. J. et al. Microbial and physicochemical characteristics of compact anaerobic ammonium-oxidizing granules in an upflow anaerobic sludge blanket reactor. Appl. Environ. Microbiol. 76, 2652-2656 (2010).
10. Gonzalez-Gil, G., Sougrat, R., Behzad, A. R., Lens, P. N. L. & Saikaly, P. E. Microbial community composition and ultrastructure of granules from a full-scale anammox reactor. Microb. Ecol. 70, 118-131 (2014).
11. Hou, X., Liu, S. & Zhang, Z. Role of extracellular polymeric substance in determining the high aggregation ability of anammox sludge. Water Res. 75, 51-62 (2015).
12. Ali, M. et al. Physiological characterization of anaerobic ammonium oxidizing bacterium Candidatus Jettenia caeni. Environ. Microbiol. 17, 2172-2189 (2015).
13. Ma, Y., Sundar, S., Park, H. & Chandran, K. The effect of inorganic carbon on microbial interactions in a biofilm nitritation-Anammox process. Water Res. 70, 246-254 (2015).
14. Li, X. R. et al. The bacterial diversity in an anaerobic ammonium-oxidizing (anammox) reactor community. Syst. Appl. Microbiol. 32, 278-289 2009
15. Gonzalez-Martinez, A. et al. Microbial community analysis of a full-scale DEMON bioreactor. Bioprocess Biosyst. Eng. 38, 499-508 (2015).
16. Speth, D. R., in t Zandt, M. H., Guerrero-Cruz, S., Dutilh, B. E. & Jetten, M. S. M. Genome-based microbial ecology of anammox granules in a full-scale wastewater treatment system. Nat. Commun. 7, 11172 (2016).
17. Ni, B. J., Ruscalleda, M. & Smets, B. F. Evaluation on the microbial interactions of anaerobic ammonium oxidizers and heterotrophs in Anammox biofilm. Water Res. 46, 4645-4652 (2012).
18. Liu, Y. et al. Assessment of heterotrophic growth supported by soluble microbial products in anammox biofilm using multidimensional modeling. Sci. Rep. 6, 27576 (2016).
19. Lawson, C. E. et al. Rare taxa have potential to make metabolic contributions in enhanced biological phosphorus removal ecosystems. Environ. Microbiol. 17, 4979-4993 (2015).
20. Konwar, K. M. et al. MetaPathways v2.5: quantitative functional, taxonomic and usability improvements. Bioinformatics 31, 3345-3347 2015:
21. Maalcke, W. J. et al. Structural basis of biological no generation by octaheme oxidoreductases. J. Biol. Chem. 289, 1228-1242 (2014).
22. Schalk, J., De Vries, S., Kuenen, J. G. & Jetten, M. S. M. Involvement of a novel hydroxylamine oxidoreductase in anaerobic ammonium oxidation. Biochemistry 39, 5405-5412 (2000).
23. Shimamura, M. et al. Another multiheme protein, hydroxylamine oxidoreductase, abundantly produced in an anammox bacterium besides the hydrazine-oxidizing enzyme. J. Biosci. Bioeng. 105, 243-248 2008
24. Oshiki, M., Shinyako-Hata, K., Satoh, H. & Okabe, S. Draft genome sequence of an anaerobic ammonium-oxidizing bacterium, Candidatus Brocadia sinica. Genome Announc. 3, 3-4 (2015).
25. Ferousi, C. et al. Identification of the type II cytochrome c maturation pathway in anammox bacteria by comparative genomics. BMC Microbiol. 13, 265 (2013).
26. Oshiki, M., Ali, M., Shinyako-Hata, K., Satoh, H. & Okabe, S. Hydroxylaminedependent anaerobic ammonium oxidation (anammox) by Candidatus Brocadia sinica. Environ. Microbiol. 18, 3133-3143 (2016).
27. Zhang, S. & Bryant, D. The tricarboxylic acid cycle in cyanobacteria. Science 7002, 1551-1554 (2011).
28. Liu, Z. et al. Complete genome of Ignavibacterium album, a metabolically versatile, flagellated, facultative anaerobe from the phylum Chlorobi. Front. Microbiol. 3, 1-15 (2012).
29. Kadnikov, V. V. et al. Genomic analysis of Melioribacter roseus, facultatively anaerobic organotrophic bacterium representing a novel deep lineage within Bacteriodetes/Chlorobi group. PLoS ONE 8, e53047 (2013).
30. Spaans, S. K., Weusthuis, R. A., van der Oost, J. & Kengen, S. W. M. NADPH-generating systems in bacteria and archaea. Front. Microbiol. 6, 1-27 (2015).
31. Wolfe, A. J. The acetate switch. Microbiol. Mol. Biol. Rev. 69, 12-50 (2005).
32. Buckel, W. & Thauer, R. K. Energy conservation via electron bifurcating ferredoxin reduction and proton/Na translocating ferredoxin oxidation. Biochim. Biophys. Acta 1827, 94-113 (2013).
33. McDowall, J. S. et al. Bacterial formate hydrogenlyase complex. Proc. Natl Acad. Sci. USA 111, E3948-E3956 (2014).
34. Sawers, G. The hydrogenases and formate dehydrogenases of Escherichia coli. Antonie van Leeuwenhoek 66, 57-88 (1994).
35. Richardson, D. J. Bacterial respiration: A flexibe process for a changing environment. Microbiology 146, 551-571 (2000).
36. Hase, C. C. & Finkelstein, R. A. Bacterial extracellular zinc-containing metalloproteases. Microbiol. Rev. 57, 823-837 (1993).
37. Siezen, R. J. & Leunissen, J. A. Subtilases: The superfamily of subtilisin-like serine proteases. Protein Sci. 6, 501-523 (1997).
38. Akashi, H. & Gojobori, T. Metabolic efficiency and amino acid composition in the proteomes of Escherichia coli and Bacillus subtilis. Proc. Natl Acad. Sci. USA. 99, 3695-3700 (2002).
39. Mee, M. T., Collins, J. J., Church, G. M. & Wang, H. H. Syntrophic exchange in synthetic microbial communities. Proc. Natl Acad. Sci. USA 111, E2149-E2156 (2014).
40. Abma, W. R., Driessen, W., Haarhuis, R. & Van Loosdrecht, M. C. M. Upgrading of sewage treatment plant by sustainable and cost-effective separate treatment of industrial wastewater. Water Sci. Technol. 61, 1715-1722 (2010).
41. Van Mooy, B. A. S., Keil, R. G. & Devol, A. H. Impact of suboxia on sinking particulate organic carbon: Enhanced carbon flux and preferential degradation of amino acids via denitrification. Geochim. Cosmochim. Acta 66, 457-465 (2002).
42. Kindaichi, T., Yuri, S., Ozaki, N. & Ohashi, A. Ecophysiological role and function of uncultured Chloroflexi in an anammox reactor. Water Sci. Technol. 66, 2556-2561 (2012).
43. Datta, M. S., Sliwerska, E., Gore, J., Polz, M. & Cordero, O. X. Microbial interactions lead to rapid micro-scale successions on model marine particles. Nat. Commun. 7, 11965 (2016).
44. Degnan, P. H., Taga, M. E. & Goodman, A. L. Vitamin B12 as a modulator of gut microbial ecology. Cell Metab. 20, 769-778 (2014).
45. Ali, M. et al. Source identification of nitrous oxide emission pathways from a single-stage nitritation-Anammox granular reactor. Water Res. 102, 147-157 (2016).
46. Lilja, E. E. & Johnson, D. R. Segregating metabolic processes into different microbial cells accelerates the consumption of inhibitory substrates. ISME J. 10, 1568-1578 (2016).
47. Kindaichi, T. et al. In situ activity and spatial organization of anaerobic ammonium-oxidizing (anammox) bacteria in biofilms. Appl. Environ. Microbiol. 73, 4931-4939 (2007).
48. Vlaeminck, S. E. et al. Aggregate size and architecture determine microbial activity balance for one-stage partial nitritation and anammox. Appl. Environ. Microbiol. 76, 900-909 (2010).
49. Kartal, B. et al. Candidatus Brocadia fulgida: An autofluorescent anaerobic ammonium oxidizing bacterium. FEMS Microbiol. Ecol. 63, 46-55 (2008).
50. Kotay, S. M., Mansell, B. L., Hogsett, M., Pei, H. & Goel, R. Anaerobic ammonia oxidation (ANAMMOX) for side-stream treatment of anaerobic digester filtrate process performance and microbiology. Biotechnol. Bioeng. 110, 1180-1192 (2013).
51. Joshi, N. A. & Fass, J. N. Sickle: A sliding-window, adaptive, quality-based trimming tool for FastQ files Available at https://github.com/najoshi/sickle (2011).
52. Salzberg, S. L. FLASH: fast length adjustment of short reads to improve genome assemblies tanja mago. Bioinformatics 27, 2957-2963 2011
53. Kang, D. D., Froula, J., Egan, R. & Wang, Z. MetaBAT, an efficient tool for accurately reconstructing single genomes from complex microbial communities. PeerJ 3, e1165 (2015).
54. Parks, D. H., Imelfort, M., Skennerton, C. T., Hugenholtz, P. & Tyson, G. W. CheckM: Assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 25, 1043-1055 2015
55. Dupont, C. L. et al. Genomic insights to SAR86, an abundant and uncultivated marine bacterial lineage. ISME J. 6, 1186-1199 (2012).
56. Darling, A. E. et al. PhyloSift: phylogenetic analysis of genomes and metagenomes. PeerJ 2, e243 (2014).
57. Hyatt, D. et al. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11, 119 (2010).
58. Konwar, K., Hanson, N., Page, A. & Hallam, S. J. MetaPathways: A modular pipeline for constructing Pathway/Genome Databases from environmental sequence information. BMC Bioinformatics 14, 202 (2013).
59. Karp, P. D. et al. Pathway Tools version 19.0 update: software for pathway/genome informatics and systems biology. Brief. Bioinform. 17, 877-890 (2015).
60. Karp, P. D., Latendresse, M. & Caspi, R. The pathway tools pathway prediction algorithm. Stand. Genomic Sci. 5, 424-429 (2011).
61. Kopylova, E., Noe, L. & Touzet, H. SortMeRNA: Fast and accurate filtering of ribosomal RNAs in metatranscriptomic data. Bioinformatics 28, 3211-3217 (2012).
62. Konstantinidis, K. T. & Tiedje, J. M. Genomic insights that advance the species definition for prokaryotes. Proc. Natl. Acad. Sci. USA 102, 2567-2572 (2005).
63. Anders, S., Pyl, P. T. & Huber, W. HTSeq-A Python framework to work with high-Throughput sequencing data. Bioinformatics 31, 166-169 (2015).
64. Mortazavi, A., Williams, B. A., McCue, K., Schaeffer, L. & Wold, B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat. Methods 5, 621-628 (2008).
65. Lombard, V., Golaconda Ramulu, H., Drula, E., Coutinho, P. M. & Henrissat, B. The carbohydrate-Active enzymes database (CAZy) in 2013. Nucleic Acids Res. 42, 490-495 (2014).
66. Rawlings, N. D., Barrett, A. J. & Finn, R. Twenty years of the MEROPS database of proteolytic enzymes, their substrates and inhibitors. Nucleic Acids Res. 44, D343-D350 (2015).
67. Marchler-Bauer, A. et al. CDD: NCBIs conserved domain database. Nucleic Acids Res. 43, D222-D226 (2015).
68. Finn, R. D. et al. The Pfam protein families database: Towards a more sustainable future. Nucleic Acids Res. 44, D279-D285 (2016).
69. Yu, C.-S., Lin, C.-J. & Hwang, J.-K. Predicting subcellular localization of proteins for Gram-negative bacteria by support vector machines based on n-peptide compositions. Protein Sci. 13, 1402-1406 (2004).
70. Saier, M. H. et al. The transporter classification database (TCDB): Recent advances. Nucleic Acids Res. 44, D372-D379 (2016).