Rare taxa have potential to make metabolic contributions in enhanced biological phosphorus removal ecosystems

Environmental Microbiology

Volumn 17, Issue 12, 2015, Pages 4979-4993

  Lawson, Christopher E ^a,c   Strachan, Blake J ^a   Hanson, Niels W ^a   Hahn, Aria S ^a   Hall, Eric R ^a   Rabinowitz, Barry ^a,b   Mavinic, Donald S ^a   Ramey, William D ^a   Hallam, Steven J ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b University of British Columbia ^*  (Canada)

^c University of Wisconsin Madison   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHORUS; RIBOSOME DNA; RIBOSOME RNA; WASTE WATER; WATER POLLUTANT;

BACTERIUM; BIOREACTOR; BIOREMEDIATION; CLASSIFICATION; ECOSYSTEM; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; PHYLOGENY; WASTE WATER; WATER POLLUTANT;

BACTERIA; BIODEGRADATION, ENVIRONMENTAL; BIOREACTORS; DNA, RIBOSOMAL; ECOSYSTEM; PHOSPHORUS; PHYLOGENY; RNA, RIBOSOMAL; WASTE WATER; WATER POLLUTANTS, CHEMICAL;

EID: 84955695127     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/1462-2920.12875     Document Type: Article

References (89)

1. Albertsen, M., Hansen, L.B.S., Saunders, A.M., Nielsen, P.H., and Nielsen, K.L. (2012) A metagenome of a full-scale microbial community carrying out enhanced biological phosphorus removal. ISME J 6: 1094-1106.
2. Allers, E., Wright, J.J., Konwar, K.M., Howes, C.G., Beneze, E., Hallam, S.J., and Sullivan, M.B. (2013) Diversity and population structure of Marine Group A bacteria in the Northeast subarctic Pacific Ocean. ISME J 7: 256-268.
3. Altschul, S.F., Gish, W., Miller, W., Myers, E.W., and Lipman, D.J. (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
4. APHA (2005) Standard Methods for the Examination of Water and Waste Water. Washington, DC: American Public Health Association, American Water Works Association and Water Environment Federation.
5. Barnard, R.L., Osborne, C.A., and Firestone, M.K. (2013) Responses of soil bacterial and fungal communities to extreme desiccation and rewetting. ISME J 7: 2229-2241.
6. Berdjeb, L., Pollet, T., Domaizon, I., and Jacquet, S. (2011) Effect of grazers and viruses on bacterial community structure and production in two contrasting trophic lakes. BMC Microbiol 11: 88.
7. Blazewicz, S.J., Barnard, R.L., Daly, R.A., and Firestone, M.K. (2013) Evaluating rRNA as an indicator of microbial activity in environmental communities: limitations and uses. ISME J 7: 2061-2068.
8. Braeken, K., Moris, M., Daniels, R., Vanderleyden, J., and Michiels, J. (2006) New horizons for (p)ppGpp in bacterial and plant physiology. Trends Microbiol 14: 45-54.
9. Campbell, B.J., and Kirchman, D.L. (2013) Bacterial diversity, community structure and potential growth rates along an estuarine salinity gradient. ISME J 7: 210-220.
10. Campbell, B.J., Yu, L., Heidelberg, J.F., and Kirchman, D.L. (2011) Activity of abundant and rare bacteria in a coastal ocean. PNAS 108: 12776-12781.
11. Caporaso, J.G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F.D., Costello, E.K., etal. (2010) QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7: 335-336.
12. Crosby, L.D., and Criddle, C.S. (2003) Understanding bias in microbial community analysis techniques due to rrn operon copy number heterogeneity. Biotechniques 34: 790-803.
13. Dolinšek, J., Lagkouvardos, I., Wanek, W., Wagner, M., and Daims, H. (2013) Interactions of nitrifying bacteria and heterotrophs: identification of a Micavibrio-like putative predator of Nitrospira spp. Appl Environ Microbiol 79: 2027-2037.
14. Engelbrektson, A., Kunin, V., Wrighton, K.C., Zvenigorodsky, N., Chen, F., Ochman, H., and Hugenholtz, P. (2010) Experimental factors affecting PCR-based estimates of microbial species richness and evenness. ISME J 4: 642-647.
15. Eschenhagen, M., Schuppler, M., and Röske, I. (2003) Molecular characterization of the microbial community structure in two activated sludge systems for the advanced treatment of domestic effluents. Water Res 37: 3224-3232.
16. Evans, T.N., and Seviour, R.J. (2012) Estimating biodiversity of fungi in activated sludge communities using culture-independent methods. Microbial Ecol 63: 773-786.
17. Flardh, K., Cohen, P.S., and Kjellebergl, S. (1992) Ribosomes exist in large excess over the apparent demand for protein synthesis during carbon starvation in marine Vibrio sp. strain CCUG 15956. J Bacteriol 174: 6780-6788.
18. Flowers, J.J., Cadkin, T.A., and McMahon, K.D. (2013a) Seasonal bacterial community dynamics in a full-scale enhanced biological phosphorus removal plant. Water Res 47: 7019-7031.
19. Flowers, J.J., He, S., Malfatti, S., del Rio, T.G., Tringe, S.G., Hugenholtz, P., and McMahon, K.D. (2013b) Comparative genomics of two 'Candidatus Accumulibacter' clades performing biological phosphorus removal. ISME J 7: 2301-2314.
20. Galand, P.E., Casamayor, E.O., Kirchman, D.L., and Lovejoy, C. (2009) Ecology of the rare microbial biosphere of the Arctic Ocean. PNAS 106: 22427-22432.
21. García Martín, H., Ivanova, N., Kunin, V., Warnecke, F., Barry, K.W., McHardy, A.C., etal. (2006) Metagenomic analysis of two enhanced biological phosphorus removal (EBPR) sludge communities. Nat Biotechnol 24: 1263-1269.
22. Gibbons, S.M., Caporaso, J.G., Pirrung, M., Field, D., Knight, R., and Gilbert, J.A. (2013) Evidence for a persistent microbial seed bank throughout the global ocean. PNAS 110: 4651-4655.
23. Gong, J., Dong, J., Liu, X., and Massana, R. (2013) Extremely high copy numbers and polymorphisms of the rDNA operon estimated from single cell analysis of oligotrich and peritrich ciliates. Protist 164: 369-379.
24. Gourse, R.L., Gaal, T., Bartlett, M.S., Appleman, J.A., and Ross, W. (1996) rRNA transcription and growth rate-dependent regulation of ribosome synthesis in Escherichia coli. Annu Rev Microbiol 50: 645-677.
25. Gray, N.D., Miskin, I.P., Kornilova, O., Curtis, T.P., and Head, I.M. (2002) Occurrence and activity of Archaea in aerated activated sludge wastewater treatment plants. Environ Microbiol 4: 158-168.
26. Gruber-Dorninger, C., Pester, M., Kitzinger, K., Savio, D.F., Loy, A., Rattei, T., etal. (2014) Functionally relevant diversity of closely related Nitrospira in activated sludge. ISME J 9: 643-655.
27. Hall, E.R., Monti, A., and Mohn, W.W. (2010) A comparison of bacterial populations in enhanced biological phosphorus removal processes using membrane filtration or gravity sedimentation for solids-liquid separation. Water Res 44: 2703-2714.
28. He, S., and McMahon, K.D. (2011a) 'Candidatus Accumulibacter' gene expression in response to dynamic EBPR conditions. ISME J 5: 329-340.
29. He, S., and McMahon, K.D. (2011b) Microbiology of 'Candidatus Accumulibacter' in activated sludge. Microbial Biotechnol 4: 603-619.
30. He, S., Gall, D.L., and McMahon, K.D. (2007) 'Candidatus Accumulibacter' population structure in enhanced biological phosphorus removal sludges as revealed by polyphosphate kinase genes. Appl Environ Microbiol 73: 5865-5874.
31. He, S., Kunin, V., Haynes, M., Martin, H.G., Ivanova, N., Rohwer, F., etal. (2010) Metatranscriptomic array analysis of 'Candidatus Accumulibacter phosphatis'-enriched enhanced biological phosphorus removal sludge. Environ. Microbiol. 12: 1205-1217.
32. Henriques, I.D.S., and Love, N.G. (2007) The role of extracellular polymeric substances in the toxicity response of activated sludge bacteria to chemical toxins. Water Res 41: 4177-4185.
33. Hu, M., Wang, X., Wen, X., and Xia, Y. (2012) Microbial community structures in different wastewater treatment plants as revealed by 454-pyrosequencing analysis. Bioresour Technol 117: 72-79.
34. Hugoni, M., Taib, N., Debroas, D., Domaizon, I., Jouan Dufournel, I., Bronner, G., etal. (2013) Structure of the rare archaeal biosphere and seasonal dynamics of active ecotypes in surface coastal waters. PNAS 110: 6004-6009.
35. Hunt, D.E., Lin, Y., Church, M.J., Karl, D.M., Tringe, S.G., Izzo, L.K., and Johnson, Z.I. (2013) Relationship between abundance and specific activity of bacterioplankton in open ocean surface waters. Appl Environ Microbiol 79: 177-184.
36. Jones, S.E., and Lennon, J.T. (2010) Dormancy contributes to the maintenance of microbial diversity. PNAS 107: 5881-5886.
37. Kim, B.-C., Kim, S., Shin, T., Kim, H., and Sang, B.-I. (2013a) Comparison of the bacterial communities in anaerobic, anoxic, and oxic chambers of a pilot A(2)O process using pyrosequencing analysis. Curr Microbiol 66: 555-565.
38. Kim, J.M., Lee, H.J., Lee, D.S., and Jeon, C.O. (2013b) Characterization of the denitrification-associated phosphorus uptake properties of 'Candidatus Accumulibacter phosphatis' clades in sludge subjected to enhanced biological phosphorus removal. Appl Environ Microbiol 79: 1969-1979.
39. Kim, T.-S., Jeong, J.-Y., Wells, G.F., and Park, H.-D. (2013c) General and rare bacterial taxa demonstrating different temporal dynamic patterns in an activated sludge bioreactor. Appl Microbiol Biotechnol 97: 1755-1765.
40. Kong, Y., Nielsen, J.L., and Halkjær, P. (2005) Identity and ecophysiology of uncultured actinobacterial polyphosphate-accumulating organisms in full-scale enhanced biological phosphorus removal plants. Appl Environ Microbiol 71: 4076-4085.
41. Kong, Y., Xia, Y., and Nielsen, P.H. (2008) Activity and identity of fermenting microorganisms in full-scale biological nutrient removing wastewater treatment plants. Environ Microbiol 10: 2008-2019.
42. Kragelund, C., Remesova, Z., Nielsen, J.L., Thomsen, T.R., Eales, K., Seviour, R., etal. (2007) Ecophysiology of mycolic acid-containing Actinobacteria (Mycolata) in activated sludge foams. FEMS Microbiol Ecol 61: 174-184.
43. Kunin, V., He, S., Warnecke, F., Peterson, S.B., Martin, H.G., Haynes, M., etal. (2008) A bacterial metapopulation adapts locally to phage predation despite global dispersal. Genome Res 18: 293-297.
44. Kunin, V., Engelbrektson, A., Ochman, H., and Hugenholtz, P. (2010) Wrinkles in the rare biosphere: pyrosequencing errors. Environ Microbiol 12: 118-123.
45. Legendre, P., and Legendre, L. (1998) Numerical Ecology. Amsterdam, the Netherlands: Elsevier Science, BV.
46. Legendre, P., Oksanen, J., and ter Braak, C.J.F. (2011) Testing the significance of canonical axes in redundancy analysis. Methods Ecol Evol 2: 269-277.
47. Lennon, J.T., and Jones, S.E. (2011) Microbial seed banks: the ecological and evolutionary implications of dormancy. Nat Rev Microbiol 9: 119-130.
48. Lepp, P., and Schmidt, T. (1998) Nucleic acid content of synechococcus spp. during growth in continuous light and light/dark cycles. Archives Microbiol 170: 201-207.
49. McIlroy, S.J., Kristiansen, R., Albertsen, M., Karst, S.M., Rossetti, S., Nielsen, J.L., etal. (2013) Metabolic model for the filamentous 'Candidatus Microthrix parvicella' based on genomic and metagenomic analyses. ISME J 7: 1161-1172.
50. McMahon, K.D., and Read, E.K. (2013) Microbial contributions to phosphorus cycling in eutrophic lakes and wastewater. Ann Rev Microbiol 67: 199-219.
51. McMahon, K.D., Yilmaz, S., He, S., Gall, D.L., Jenkins, D., and Keasling, J.D. (2007) Polyphosphate kinase genes from full-scale activated sludge plants. Appl Microbiol Biotechnol 77: 167-173.
52. Martin-Fernandez, J.A., Barcelo-Vidal, C., and Pawlowsky-Glahn, V. (2003) Dealing with zeros and missing values in compositional data sets using nonparametric. Mathematical Geology 35: 253-278.
53. Mielczarek, A.T., Nguyen, H.T.T., Nielsen, J.L., and Nielsen, P.H. (2013) Population dynamics of bacteria involved in enhanced biological phosphorus removal in Danish wastewater treatment plants. Water Res 47: 1529-1544.
54. Moreno, A.M., Matz, C., Kjelleberg, S., and Manefield, M. (2010) Identification of ciliate grazers of autotrophic bacteria in ammonia-oxidizing activated sludge by RNA stable isotope probing. Appl Environ Microbiol 76: 2203-2211.
55. Morgenroth, E., Obermayer, A., Arnold, E., Brühl, A., Wagner, M., and Wilderer, P.A. (2000) Effect of long-term idle periods on the performance of sequencing batch reactors. Water Sci Technol 41: 105-114.
56. Neethling, J., Bakke, B., Benisch, M., Gu, A., and Stephens, H. (2005) Factors influencing the reliability of enhanced biological phosphorus removal. Report 01CTS3. Alexandria, VA: Water Environment Research Foundation.
57. Neufeld, J.D., Chen, Y., Dumont, M.G., and Murrell, J.C. (2008) Marine methylotrophs revealed by stable-isotope probing, multiple displacement amplification and metagenomics. Environ Microbiol 10: 1526-1535.
58. Nielsen, J.L., Nguyen, H., Meyer, R.L., and Nielsen, P.H. (2012a) Identification of glucose-fermenting bacteria in a full-scale enhanced biological phosphorus removal plant by stable isotope probing. Microbiology 158: 1818-1825.
59. Nielsen, P.H., Mielczarek, A.T., Kragelund, C., Nielsen, J.L., Saunders, A.M., Kong, Y., etal. (2010) A conceptual ecosystem model of microbial communities in enhanced biological phosphorus removal plants. Water Res 44: 5070-5088.
60. Nielsen, P.H., Saunders, A.M., Hansen, A.A., Larsen, P., and Nielsen, J.L. (2012b) Microbial communities involved in enhanced biological phosphorus removal from wastewater - a model system in environmental biotechnology. Curr Opin Biotechnol 23: 452-459.
61. Nomura, M., Gourse, R., and Baughman, G. (1984) Regulation of the synthesis of ribosomes and ribosomal components. Annu Rev Biochem 53: 75-117.
62. Oda, Y., Slagman, S., Meijer, W.G., Forney, L.J., and Gottschal, J.C. (2000) Influence of growth rate and starvation on fluorescent in situ hybridization of Rhodopseudomonas palustris. FEMS Microbiol Ecol 32: 205-213.
63. Osaka, T., Yoshie, S., Tsuneda, S., Hirata, A., Iwami, N., and Inamori, Y. (2006) Identification of acetate- or methanol-assimilating bacteria under nitrate-reducing conditions by stable-isotope probing. Microbial Ecol 52: 253-266.
64. Pedrós-Alió, C. (2006) Marine microbial diversity: can it be determined? Trends Microbiol 14: 257-263.
65. Pedrós-Alió, C. (2012) The rare bacterial biosphere. Ann Rev Mar Sci 4: 449-466.
66. Pester, M., Bittner, N., Deevong, P., Wagner, M., and Loy, A. (2010) A 'rare biosphere' microorganism contributes to sulfate reduction in a peatland. ISME J 4: 1591-1602.
67. Pradeep Ram, A.S., and Sime-Ngando, T. (2008) Functional responses of prokaryotes and viruses to grazer effects and nutrient additions in freshwater microcosms. ISME J 2: 498-509.
68. Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., etal. (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41: D590-D596.
69. Ramette, A. (2007) Multivariate analyses in microbial ecology. FEMS Microbiol Ecol 62: 142-160.
70. Rodríguez-Blanco, A., Ghiglione, J.-F., Catala, P., Casamayor, E.O., and Lebaron, P. (2009) Spatial comparison of total vs. active bacterial populations by coupling genetic fingerprinting and clone library analyses in the NW Mediterranean Sea. FEMS Microbiol Ecol 67: 30-42.
71. Russell, J.B., and Cook, G.M. (1995) Energetics of bacterial growth: balance of anabolic and catabolic reactions. Microbiol Rev 59: 48-62.
72. Saunders, A.M., Larsen, P., and Nielsen, P.H. (2013) Comparison of nutrient-removing microbial communities in activated sludge from full-scale MBRs and conventional plants. Water Sci and Technol 68: 366-371.
73. Schmid, M., Schmitz-Esser, S., Jetten, M., and Wagner, M. (2001) 16S-23S rDNA intergenic spacer and 23S rDNA of anaerobic ammonium-oxidizing bacteria: implications for phylogeny and in situ detection. Environ Microbiol 3: 450-459.
74. Shade, A., and Gilbert, J.A. (2015) Temporal patterns of rarity provide a more complete view of microbial diversity. Trends Microbiol: 1-6.
75. Shade, A., and Handelsman, J. (2012) Beyond the Venn diagram: the hunt for a core microbiome. Environ Microbiol 14: 4-12.
76. Shade, A., Hogan, C.S., Klimowicz, A.K., Linske, M., McManus, P.S., and Handelsman, J. (2012) Culturing captures members of the soil rare biosphere. Environ Microbiol 14: 2247-2252.
77. Shade, A., Jones, S.E., Caporaso, J.G., Handelsman, J., Knight, R., Fierer, N., and Gilbert, A. (2014) Conditionally rare taxa disproportionately contribute to temporal changes in microbial diversity. MBio 5: 1-9.
78. Shapiro, B.J., and Polz, M.F. (2014) Ordering microbial diversity into ecologically and genetically cohesive units. Trends in Microbiol 22: 235-247.
79. Sharp, J.H., Yoshiyama, K., Parker, A.E., Schwartz, M.C., Curless, S.E., Beauregard, A.Y., etal. (2009) A biogeochemical view of estuarine eutrophication: seasonal and spatial trends and correlations in the Delaware estuary. Estuaries and Coasts 32: 1023-1043.
80. Silva, A.F., Carvalho, G., Oehmen, A., Lousada-Ferreira, M., van Nieuwenhuijzen, A., Reis, M.A.M., and Crespo, M.T.B. (2012) Microbial population analysis of nutrient removal-related organisms in membrane bioreactors. Appl Microbiol Biotechnol 93: 2171-2180.
81. Sogin, M.L., Morrison, H.G., Huber, J.A., Mark Welch, D., Huse, S.M., Neal, P.R., etal. (2006) Microbial diversity in the deep sea and the underexplored 'rare biosphere'. PNAS 103: 12115-12120.
82. Thomsen, T.R., Kong, Y., and Nielsen, P.H. (2007) Ecophysiology of abundant denitrifying bacteria in activated sludge. FEMS Microbiol Ecol 60: 370-382.
83. Wagner, M., Rath, G., Amann, R., Koops, H.-P., and Schleifer, K.-H. (1995) In situ identification of ammonia-oxidizing bacteria. Syst Appl Microbiol 18: 251-264.
84. Wan, C.-Y., De Wever, H., Diels, L., Thoeye, C., Liang, J.-B., and Huang, L.-N. (2011) Biodiversity and population dynamics of microorganisms in a full-scale membrane bioreactor for municipal wastewater treatment. Water Res 45: 1129-1138.
85. Wexler, M., Richardson, D.J., and Bond, P.L. (2009) Radiolabelled proteomics to determine differential functioning of Accumulibacter during the anaerobic and aerobic phases of a bioreactor operating for. Environ Microbiol 11: 3029-3044.
86. Wilhelm, L., Besemer, K., Fasching, C., Urich, T., Singer, G.A., Quince, C., and Battin, T.J. (2014) Rare but active taxa contribute to community dynamics of benthic biofilms in glacier-fed streams. Environ Microbiol 16: 2514-2524. doi:10.1111/1462-2920.12392.
87. Wilmes, P., Andersson, A.F., Lefsrud, M.G., Wexler, M., Shah, M., Zhang, B., etal. (2008) Community proteogenomics highlights microbial strain-variant protein expression within activated sludge performing enhanced biological phosphorus removal. ISME J 2: 853-864.
88. Zhang, T., Shao, M.-F., and Ye, L. (2012) 454 pyrosequencing reveals bacterial diversity of activated sludge from 14 sewage treatment plants. ISME J 6: 1137-1147.
89. Zhou, J., Wu, L., Deng, Y., Zhi, X., Jiang, Y.-H., Tu, Q., etal. (2011) Reproducibility and quantitation of amplicon sequencing-based detection. ISME J 5: 1303-1313.