A Physiological and Genomic Comparison of Nitrosomonas Cluster 6a and 7 Ammonia-Oxidizing Bacteria

  • Christopher J. Sedlacek
  • Brian McGowan
  • Yuichi Suwa
  • Luis Sayavedra-Soto
  • Hendrikus J. Laanbroek
  • Lisa Y. Stein
  • Jeanette M. Norton
  • Martin G. Klotz
  • Annette BollmannEmail author
Genes and Genomes


Ammonia-oxidizing bacteria (AOB) within the genus Nitrosomonas perform the first step in nitrification, ammonia oxidation, and are found in diverse aquatic and terrestrial environments. Nitrosomonas AOB were grouped into six defined clusters, which correlate with physiological characteristics that contribute to adaptations to a variety of abiotic environmental factors. A fundamental physiological trait differentiating Nitrosomonas AOB is the adaptation to either low (cluster 6a) or high (cluster 7) ammonium concentrations. Here, we present physiological growth studies and genome analysis of Nitrosomonas cluster 6a and 7 AOB. Cluster 6a AOB displayed maximum growth rates at ≤ 1 mM ammonium, while cluster 7 AOB had maximum growth rates at ≥ 5 mM ammonium. In addition, cluster 7 AOB were more tolerant of high initial ammonium and nitrite concentrations than cluster 6a AOB. Cluster 6a AOB were completely inhibited by an initial nitrite concentration of 5 mM. Genomic comparisons were used to link genomic traits to observed physiological adaptations. Cluster 7 AOB encode a suite of genes related to nitrogen oxide detoxification and multiple terminal oxidases, which are absent in cluster 6a AOB. Cluster 6a AOB possess two distinct forms of ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO) and select species encode genes for hydrogen or urea utilization. Several, but not all, cluster 6a AOB can utilize urea as a source of ammonium. Hence, although Nitrosomonas cluster 6a and 7 AOB have the capacity to fulfill the same functional role in microbial communities, i.e., ammonia oxidation, differentiating species-specific and cluster-conserved adaptations is crucial in understanding how AOB community succession can affect overall ecosystem function.


Ammonia-oxidizing bacteria Nitrosomonas Nitrification Niche differentiation Ammonium availability 



We thank the Center for Genome Research and Biocomputing (CGRB) at Oregon State University for the sequencing services, the Center for Bioinformatics and Functional Genomics at Miami University for access to CLC workbench, and Dr. Petra Pjevac for assistance with phylogenomics.


This work was funded by start-up funds from Miami University to A Bollmann, a National Science Foundation grant (DEB-1120443) to A Bollmann, a NSF Research Coordination Network grant 0541797 (Nitrification) to DJ Arp, WJ Hickey, MG Klotz, JM Norton, and BB Ward, Miami University Undergraduate Research Awards to B McGowan, and Utah Agricultural Experiment Station, Utah State University to JM Norton.

Supplementary material

248_2019_1378_MOESM1_ESM.docx (36 kb)
Supplementary Table 1 (DOCX 35 kb)
248_2019_1378_MOESM2_ESM.docx (13 kb)
Supplementary Table 2 (DOCX 13 kb)


  1. 1.
    Breisha GZ, Winter J (2010) Bio-removal of nitrogen from wastewaters—a review. Am Sci 8:210–228Google Scholar
  2. 2.
    Mancino CF, Troll J (1990) Nitrate and ammonium leaching losses from N fertilizers applied to ‘Penncross’ creeping bentgrass. Hortic Sci 25:194–196. Google Scholar
  3. 3.
    Anderson DM, Glibert PM, Burkholder JM (2002) Harmful algal blooms and eutrophication: nutrient sources, composition, and consequences. Estuaries 25:704–726. CrossRefGoogle Scholar
  4. 4.
    Justić D, Rabalais NN, Turner RE, Dortch Q (1995) Changes in nutrient structure of river-dominated coastal waters: stoichiometric nutrient balance and its consequences. Estuar Coast Shelf Sci 40:339–356. CrossRefGoogle Scholar
  5. 5.
    Justić D, Rabalais NN, Turner RE (1995) Stoichiometric nutrient balance and origin of coastal eutrophication. Mar Pollut Bull 30:41–46. CrossRefGoogle Scholar
  6. 6.
    Kozlowski JA, Price J, Stein LY (2014) Revision of N2O-producing pathways in the ammonia-oxidizing bacterium Nitrosomonas europaea ATCC 19718. Appl Environ Microbiol 80:4930–4935. CrossRefGoogle Scholar
  7. 7.
    Hink L, Lycus P, Gubry-Rangin C, Frostegård Å, Nicol GW, Prosser JI, Bakken LR (2017) Kinetics of NH3-oxidation, NO-turnover, N2O-production and electron flow during oxygen depletion in model bacterial and archaeal ammonia oxidisers. Environ Microbiol 19:4882–4896. CrossRefGoogle Scholar
  8. 8.
    Koops H, Purkhold U, Pommerening-Roeser A et al (2006) The lithoautotrophic ammonia-oxidizing bacteria. Prokaryotes 5:778–811CrossRefGoogle Scholar
  9. 9.
    Stahl DA, de la Torré JR (2012) Physiology and diversity of ammonia-oxidizing archaea. Annu Rev Microbiol 66:83–101. CrossRefGoogle Scholar
  10. 10.
    Daims H, Lücker S, Wagner M (2016) A new perspective on microbes formerly known as nitrite-oxidizing bacteria. Trends Microbiol 24:699–712. CrossRefGoogle Scholar
  11. 11.
    Daims H, Lebedeva EV, Pjevac P, Han P, Herbold C, Albertsen M, Jehmlich N, Palatinszky M, Vierheilig J, Bulaev A, Kirkegaard RH, von Bergen M, Rattei T, Bendinger B, Nielsen PH, Wagner M (2015) Complete nitrification by Nitrospira bacteria. Nature 528:504–509. CrossRefGoogle Scholar
  12. 12.
    van Kessel MAHJ, Speth DR, Albertsen M, Nielsen PH, op den Camp HJM, Kartal B, Jetten MSM, Lücker S (2015) Complete nitrification by a single microorganism. Nature 528:555–559. CrossRefGoogle Scholar
  13. 13.
    Parks DH, Chuvochina M, Waite DW, Rinke C, Skarshewski A, Chaumeil PA, Hugenholtz P (2018) A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Nat Biotechnol 36:996–1004. Google Scholar
  14. 14.
    Purkhold U, Pommerening-Roeser A, Juretschko S et al (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 66:5368–5382CrossRefGoogle Scholar
  15. 15.
    Prosser JI, Head IM, Stein LY (2014) The family Nitrosomonadaceae. In: Rosenberg E, DeLongEF LS, Stackebrandt E, Thompson F (eds) The prokaryotes: Alphaproteobacteria and Betaproteobacteria4th edn. Springer, Berlin Heidelberg, pp 901–918CrossRefGoogle Scholar
  16. 16.
    Stephen J, McCaig A, Smith Z et al (1996) Molecular diversity of soil and marine 16S rRNA gene sequences related to beta-subgroup ammonia-oxidizing bacteria. Appl Environ Microbiol 62:4147–4154Google Scholar
  17. 17.
    Kowalchuk G, Stephen J, DeBoer W et al (1997) Analysis of ammonia-oxidizing bacteria of the beta subdivision of the class Proteobacteria in coastal sand dunes by denaturing gradient gel electrophoresis and sequencing of PCR-amplified 16S ribosomal DNA fragments. Appl Environ Microbiol 63:1489–1497Google Scholar
  18. 18.
    Koops H, Pommerening-Roser A (2001) Distribution and ecophysiology of the nitrifying bacteria emphasizing cultured species 37:1–9.
  19. 19.
    García-Ríos E, López-Malo M, Guillamón JM (2014) Global phenotypic and genomic comparison of two Saccharomyces cerevisiae wine strains reveals a novel role of the sulfur assimilation pathway in adaptation at low temperature fermentations. BMC Genomics 15:1059. CrossRefGoogle Scholar
  20. 20.
    Rocap G, Larimer FW, Lamerdin J, Malfatti S, Chain P, Ahlgren NA, Arellano A, Coleman M, Hauser L, Hess WR, Johnson ZI, Land M, Lindell D, Post AF, Regala W, Shah M, Shaw SL, Steglich C, Sullivan MB, Ting CS, Tolonen A, Webb EA, Zinser ER, Chisholm SW (2003) Genome divergence in two Prochlorococcus ecotypes reflects oceanic niche differentiation. Nature 424:1042–1047. CrossRefGoogle Scholar
  21. 21.
    Herbold CW, Morley LEL, Jung M-Y et al (2017) Ammonia-oxidizing archaea living at low pH: insights from comparative genomics. Environ Microbiol 19:4939–4952. CrossRefGoogle Scholar
  22. 22.
    Arp DJ, Chain PSG, Klotz MG (2007) The impact of genome analyses on our understanding of ammonia-oxidizing bacteria. Annu Rev Microbiol 61:503–528. CrossRefGoogle Scholar
  23. 23.
    Bollmann A, Sedlacek CJ, Norton J, Laanbroek HJ, Suwa Y, Stein LY, Klotz MG, Arp D, Sayavedra-Soto L, Lu M, Bruce D, Detter C, Tapia R, Han J, Woyke T, Lucas SM, Pitluck S, Pennacchio L, Nolan M, Land ML, Huntemann M, Deshpande S, Han C, Chen A, Kyrpides N, Mavromatis K, Markowitz V, Szeto E, Ivanova N, Mikhailova N, Pagani I, Pati A, Peters L, Ovchinnikova G, Goodwin LA (2013) Complete genome sequence of Nitrosomonas sp. Is79, an ammonia oxidizing bacterium adapted to low ammonium concentrations. Stand Genomic Sci 7:469–482. Google Scholar
  24. 24.
    Suwa Y, Sumino T, Noto K (1997) Phylogenetic relationships of activated sludge isolates of ammonia oxidizers with different sensitivities to ammonium sulfate. J Gen Appl Microbiol 43:373–379. CrossRefGoogle Scholar
  25. 25.
    Koops HP, Bottcher B, Möller UC et al (1991) Classification of eight new species of ammonia-oxidizing bacteria: Nitrosomonas communis sp. nov., Nitrosomonas ureae sp. nov., Nitrosomonas aestuarii sp. nov., Nitrosomonas marina sp. nov., Nitrosomonas nitrosa sp. nov., Nitrosomonas eutropha sp. nov., Nitrosomonas oligotropha sp. nov. and Nitrosomonas halophila sp. nov. Microbiology 137:1689–1699. Google Scholar
  26. 26.
    Suwa Y, Imamura Y, Suzuki T et al (1994) Ammonia-oxidizing bacteria with different sensitivities to (NH4)2SO4 in activated sludges. Water Res 28:1523–1532. CrossRefGoogle Scholar
  27. 27.
    Verhagen F, Laanbroek H (1991) Competition for ammonium between nitrifying and heterotrophic bacteria in dual energy-limited chemostats. Appl Environ Microbiol 57:3255–3263Google Scholar
  28. 28.
    Bollmann A, French E, Laanbroek HJ (2011) Isolation, cultivation, and characterization of ammonia-oxidizing bacteria and archaea adapted to low ammonium concentrations. Methods Enzymol 486:55–88. CrossRefGoogle Scholar
  29. 29.
    Kandeler E, Gerber H (1988) Short-term assay of soil urease activity using colorimetric determination of ammonium. Biol Fertil Soils 6:68–72CrossRefGoogle Scholar
  30. 30.
    Keeney DR, Nelson DW (1982) Nitrogen—inorganic forms. In: Page AL (ed) Methods in soil analysis—part 2. American Society of Agronomy, Madison, pp 643–698Google Scholar
  31. 31.
    Belser L, Schmidt E (1980) Growth and oxidation kinetics of three genera of ammonia-oxidizing nitrifiers. FEMS Microbiol Lett 7:213–216. CrossRefGoogle Scholar
  32. 32.
    Seemann T (2014) Prokka: rapid prokaryotic genome annotation. Bioinformatics 30:2068–2069. CrossRefGoogle Scholar
  33. 33.
    Chen I-MA, Markowitz VM, Chu K, Palaniappan K, Szeto E, Pillay M, Ratner A, Huang J, Andersen E, Huntemann M, Varghese N, Hadjithomas M, Tennessen K, Nielsen T, Ivanova NN, Kyrpides NC (2017) IMG/M: integrated genome and metagenome comparative data analysis system. Nucleic Acids Res 45:D507–D516. CrossRefGoogle Scholar
  34. 34.
    Vallenet D, Belda E, Calteau A, Cruveiller S, Engelen S, Lajus A, le Fèvre F, Longin C, Mornico D, Roche D, Rouy Z, Salvignol G, Scarpelli C, Thil Smith AA, Weiman M, Médigue C (2013) MicroScope—an integrated microbial resource for the curation and comparative analysis of genomic and metabolic data. Nucleic Acids Res 41:D636–D647. CrossRefGoogle Scholar
  35. 35.
    Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW (2015) CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res 25:1043–1055. CrossRefGoogle Scholar
  36. 36.
    Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. CrossRefGoogle Scholar
  37. 37.
    Bollmann A, Bar-Gilissen M, Laanbroek H (2002) Growth at low ammonium concentrations and starvation response as potential factors involved in niche differentiation among ammonia-oxidizing bacteria. Appl Environ Microbiol 68:4751–4757CrossRefGoogle Scholar
  38. 38.
    Martens-Habbena W, Berube PM, Urakawa H, de la Torre JR, Stahl DA (2009) Ammonia oxidation kinetics determine niche separation of nitrifying archaea and bacteria. Nature 461:976–979. CrossRefGoogle Scholar
  39. 39.
    Schramm A, de Beer D, van den Heuvel JC et al (1999) Micro-environments and mass transfer phenomena in biofilms studied with microsensors. Water Sci Technol 39:173–178. Google Scholar
  40. 40.
    Jung M-Y, Park S-J, Min D, Kim JS, Rijpstra WIC, Sinninghe Damsté JS, Kim GJ, Madsen EL, Rhee SK (2011) Enrichment and characterization of an autotrophic ammonia-oxidizing archaeon of mesophilic crenarchaeal group I.1a from an agricultural soil. Appl Environ Microbiol 77:8635–8647. CrossRefGoogle Scholar
  41. 41.
    Hayatsu M, Tago K, Uchiyama I, Toyoda A, Wang Y, Shimomura Y, Okubo T, Kurisu F, Hirono Y, Nonaka K, Akiyama H, Itoh T, Takami H (2017) An acid-tolerant ammonia-oxidizing γ-proteobacterium from soil. ISME J 11:1130–1141. CrossRefGoogle Scholar
  42. 42.
    Suzuki I, Dular U, Kwok S (1974) Ammonia and ammonium ion as substrate for oxidation of Nitrosomonas europaea cells and extracts. J Bacteriol 120:556–558Google Scholar
  43. 43.
    Laanbroek HJ, Bodelier P, Gerards S (1994) Oxygen consumption kinetics of Nitrosomonas europaea and Nitrobacter hamburgensis grown in mixed continuous cultures at different oxygen concentrations. Arch Microbiol 161:156–162CrossRefGoogle Scholar
  44. 44.
    Bollmann A, Schmidt I, Saunders A, Nicolaisen M (2005) Influence of starvation on potential ammonia-oxidizing activity and amoA mRNA levels of Nitrosospira briensis. Appl Environ Microbiol 71:1276–1282CrossRefGoogle Scholar
  45. 45.
    Stehr G, Bottcher B, Dittberner P et al (1995) The ammonia-oxidizing nitrifying population of the river Elbe estuary. FEMS Microbiol Ecol 17:177–186. CrossRefGoogle Scholar
  46. 46.
    Sedlacek CJ, Nielsen S, Greis KD, Haffey WD, Revsbech NP, Ticak T, Laanbroek HJ, Bollmann A (2016) The effect of bacterial community members on the proteome of the ammonia-oxidizing bacterium Nitrosomonas sp. Is79. Appl Environ Microbiol 82:4776–4788. CrossRefGoogle Scholar
  47. 47.
    Kits KD, Sedlacek CJ, Lebedeva EV, Han P, Bulaev A, Pjevac P, Daebeler A, Romano S, Albertsen M, Stein LY, Daims H, Wagner M (2017) Kinetic analysis of a complete nitrifier reveals an oligotrophic lifestyle. Nature 549:269–272. CrossRefGoogle Scholar
  48. 48.
    Ward BB (1987) Kinetic-studies on ammonia and methane oxidation by Nitrosococcus oceanus. Arch Microbiol 147:126–133CrossRefGoogle Scholar
  49. 49.
    Yoon S-H, Ha S-M, Kwon S, Lim J, Kim Y, Seo H, Chun J (2017) Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 67:1613–1617. CrossRefGoogle Scholar
  50. 50.
    Stein LY, Arp DJ, Berube PM, Chain PSG, Hauser L, Jetten MSM, Klotz MG, Larimer FW, Norton JM, op den Camp HJM, Shin M, Wei X (2007) Whole-genome analysis of the ammonia-oxidizing bacterium, Nitrosomonas eutropha C91: implications for niche adaptation. Environ Microbiol 9:2993–3007. CrossRefGoogle Scholar
  51. 51.
    Thandar SM, Ushiki N, Fujitani H, Sekiguchi Y, Tsuneda S (2016) Ecophysiology and comparative genomics of Nitrosomonas mobilis MS1 isolated from autotrophic nitrifying granules of wastewater treatment bioreactor. Front Microbiol 7:1869. CrossRefGoogle Scholar
  52. 52.
    Chain P, Lamerdin J, Larimer F, Regala W, Lao V, Land M, Hauser L, Hooper A, Klotz M, Norton J, Sayavedra-Soto L, Arciero D, Hommes N, Whittaker M, Arp D (2003) Complete genome sequence of the ammonia-oxidizing bacterium and obligate chemolithoautotroph Nitrosomonas europaea. J Bacteriol 185:2759–2773CrossRefGoogle Scholar
  53. 53.
    Suwa Y, Yuichi S, Norton JM et al (2011) Genome sequence of Nitrosomonas sp. strain AL212, an ammonia-oxidizing bacterium sensitive to high levels of ammonia. J Bacteriol 193:5047–5048. CrossRefGoogle Scholar
  54. 54.
    Kozlowski JA, Kits KD, Stein LY (2016) Complete genome sequence of Nitrosomonas ureae strain Nm10, an oligotrophic group 6a nitrosomonad. Genome Announc 4(2):00094–00016. CrossRefGoogle Scholar
  55. 55.
    Kozlowski JA, Kits KD, Stein LY (2016) Genome sequence of Nitrosomonas communis strain Nm2, a mesophilic ammonia-oxidizing bacterium isolated from Mediterranean soil. Genome Announc 4(1):e01541–e01515. CrossRefGoogle Scholar
  56. 56.
    Rice MC, Norton JM, Stein LY, Kozlowski J, Bollmann A, Klotz MG, Sayavedra-Soto L, Shapiro N, Goodwin LA, Huntemann M, Clum A, Pillay M, Varghese N, Mikhailova N, Palaniappan K, Ivanova N, Mukherjee S, Reddy TBK, Yee Ngan C, Daum C, Kyrpides N, Woyke T (2017) Complete genome sequence of Nitrosomonas cryotolerans ATCC 49181, a phylogenetically distinct ammonia-oxidizing bacterium isolated from Arctic waters. Genome Announc 5:e00011–e00017. CrossRefGoogle Scholar
  57. 57.
    Stein LY, Campbell MA, Klotz MG (2013) Energy-mediated vs. ammonium-regulated gene expression in the obligate ammonia-oxidizing bacterium, Nitrosococcus oceani. Front Microbiol 4:277. CrossRefGoogle Scholar
  58. 58.
    Arciero D, Pierce B, Hendrich M, Hooper A (2002) Nitrosocyanin, a red cupredoxin-like protein from Nitrosomonas europaea. Biochemistry 41:1703–1709. CrossRefGoogle Scholar
  59. 59.
    Klotz MG, Arp DJ, Chain PSG, el-Sheikh AF, Hauser LJ, Hommes NG, Larimer FW, Malfatti SA, Norton JM, Poret-Peterson AT, Vergez LM, Ward BB (2006) Complete genome sequence of the marine, chemolithoautotrophic, ammonia-oxidizing bacterium Nitrosococcus oceani ATCC 19707. Appl Environ Microbiol 72:6299–6315. CrossRefGoogle Scholar
  60. 60.
    Zorz JK, Kozlowski JA, Stein LY, Strous M, Kleiner M (2018) Comparative proteomics of three species of ammonia-oxidizing bacteria. Front Microbiol 9:938. CrossRefGoogle Scholar
  61. 61.
    Lancaster KM, Caranto JD, Majer SH, Smith MA (2018) Alternative bioenergy: updates to and challenges in nitrification metalloenzymology. Joule 2:421–441. CrossRefGoogle Scholar
  62. 62.
    Caranto JD, Lancaster KM (2017) Nitric oxide is an obligate bacterial nitrification intermediate produced by hydroxylamine oxidoreductase. PNAS 114:8217–8222. CrossRefGoogle Scholar
  63. 63.
    Kozlowski JA, Kits KD, Stein LY (2016) Comparison of nitrogen oxide metabolism among diverse ammonia-oxidizing bacteria. Front Microbiol 7:1090. CrossRefGoogle Scholar
  64. 64.
    Patel RP, McAndrew J, Sellak H, White CR, Jo H, Freeman BA, Darley-Usmar VM (1999) Biological aspects of reactive nitrogen species. Biochim Biophys Acta (BBA) Bioenergetics 1411:385–400. CrossRefGoogle Scholar
  65. 65.
    Stein LY (2011) In: Ward BB, Arp DJ, Klotz MG (eds) Heterotrophic nitrification and nitrifiers denitrification. Nitrification ASM Press, Washington DC, pp 95–113Google Scholar
  66. 66.
    Kartal B, Wessels HJCT, van der Biezen E, Francoijs KJ, Jetten MSM, Klotz MG, Stein LY (2012) Effects of nitrogen dioxide and anoxia on global gene and protein expression in long-term continuous cultures of Nitrosomonas eutropha C91. Appl Environ Microbiol 78:4788–4794. CrossRefGoogle Scholar
  67. 67.
    Beaumont HJE, Lens SI, Westerhoff HV, van Spanning RJM (2005) Novel nirK cluster genes in Nitrosomonas europaea are required for NirK-dependent tolerance to nitrite. J Bacteriol 187:6849–6851. CrossRefGoogle Scholar
  68. 68.
    Beaumont H, Hommes N, Sayavedra-Soto L et al (2002) Nitrite reductase of Nitrosomonas europaea is not essential for production of gaseous nitrogen oxides and confers tolerance to nitrite. J Bacteriol 184:2557–2560. CrossRefGoogle Scholar
  69. 69.
    Cantera JJL, Stein LY (2007) Role of nitrite reductase in the ammonia-oxidizing pathway of Nitrosomonas europaea. Arch Microbiol 188:349–354. CrossRefGoogle Scholar
  70. 70.
    Norton JM, Klotz MG, Stein LY, Arp DJ, Bottomley PJ, Chain PSG, Hauser LJ, Land ML, Larimer FW, Shin MW, Starkenburg SR (2008) Complete genome sequence of Nitrosospira multiformis, an ammonia-oxidizing bacterium from the soil environment. Appl Environ Microbiol 74:3559–3572. CrossRefGoogle Scholar
  71. 71.
    Schwartz E, Gerischer U, Friedrich B (1998) Transcriptional regulation of Alcaligenes eutrophus hydrogenase genes. J Bacteriol 180:3197–3204. Google Scholar
  72. 72.
    Bock E, Schmidt I, Stuven R, Zart D (1995) Nitrogen loss caused by denitrifying Nitrosomonas cells using ammonium of hydrogen as electron donors and nitrite as electron acceptor. Arch Microbiol 163:16–20CrossRefGoogle Scholar
  73. 73.
    Ugidos A, Morales G, Rial E, Williams HD, Rojo F (2008) The coordinate regulation of multiple terminal oxidases by the Pseudomonas putida ANR global regulator. Environ Microbiol 10:1690–1702. CrossRefGoogle Scholar
  74. 74.
    Cannon GC, Bradburne CE, Aldrich HC, Baker SH, Heinhorst S, Shively JM (2001) Microcompartments in prokaryotes: carboxysomes and related polyhedra. Appl Environ Microbiol 67:5351–5361. CrossRefGoogle Scholar
  75. 75.
    Badger MR, Bek EJ (2008) Multiple Rubisco forms in proteobacteria: their functional significance in relation to CO2 acquisition by the CBB cycle. J Exp Bot 59:1525–1541. CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Christopher J. Sedlacek
    • 1
    • 2
  • Brian McGowan
    • 1
  • Yuichi Suwa
    • 3
  • Luis Sayavedra-Soto
    • 4
  • Hendrikus J. Laanbroek
    • 5
  • Lisa Y. Stein
    • 6
  • Jeanette M. Norton
    • 7
  • Martin G. Klotz
    • 8
  • Annette Bollmann
    • 1
    Email author
  1. 1.Department of MicrobiologyMiami UniversityOxfordUSA
  2. 2.Department of Microbiology and Ecosystem Science, Division of Microbial EcologyUniversity of ViennaViennaAustria
  3. 3.Department of Biological SciencesChuo UniversityTokyoJapan
  4. 4.Department of Botany and Plant PathologyOregon State UniversityCorvallisUSA
  5. 5.Department of Microbial EcologyNetherlands Institute of EcologyWageningenThe Netherlands
  6. 6.Department of Biological SciencesUniversity of AlbertaEdmontonCanada
  7. 7.Department of Plants, Soil and ClimateUtah State UniversityLoganUSA
  8. 8.School of Molecular BiosciencesWashington State UniversityRichlandUSA

Personalised recommendations