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Maintenance power requirements of anammox bacteria “Candidatus Brocadia sinica” and “Candidatus Scalindua sp.”

  • 1.

    Lackner S, Gilbert EM, Vlaeminck SE, Joss A, Horn H, van Loosdrecht MCM. Full-scale partial nitritation/anammox experience – an application survey. Water Res. 2014;55:292–303.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 2.

    Ali M, Okabe S. Anammox-based technologies for nitrogen removal: Advances in process start-up and remaining issues. Chemosphere. 2015;141:144–53.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 3.

    Ni S, Sung S, Yue Q, Gao B. Substrate removal evaluation of granular anammox process in a pilot-scale upflow anaerobic sludge blanket reactor. Ecol Eng 2012;38:30–36.

    Article 

    Google Scholar 

  • 4.

    Wang B, Peng Y, Guo Y, Yuan Y, Zhao M, Wang S. Impact of partial nitritation degree and C/N ratio on simultaneous sludge fermentation, denitrification and anammox process. Bioresour Technol. 2016;219:411–9.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 5.

    Zhang L, Narita Y, Gao L, Ali M, Oshiki M, Okabe S. Maximum specific growth rate of anammox bacteria revisited. Water Res. 2017;116:296–303.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 6.

    Zhang L, Okabe S. Ecological niche differentiation among anammox bacteria. Water Res. 2020;171:115468.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 7.

    Sun W, Xu MY, Wu WM, Guo J, Xia CY, Sun GP, et al. Molecular diversity and distribution of anammox community in sediments of the Dongjiang River, a drinking water source of Hong Kong. J Appl Microbiol. 2014;116:464–76.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 8.

    Zhu GB, Wang SY, Wang WD, Wang Y, Zhou LL, Jiang B, et al. Hotspots of anaerobic ammonium oxidation at land-freshwater interfaces. Nat Geosci. 2013;6:103–7.

    CAS 
    Article 

    Google Scholar 

  • 9.

    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;102:6478–83.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 10.

    Schmid M, 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;9:1476–84.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 11.

    Dalsgaard T, Canfield DE, Petersen J, Thamdrup B, Acuña-González J. N2 production by the anammox reaction in the anoxic water column of Golfo Dulce, Costa Rica. Nature. 2003;422:606–8.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 12.

    Kuypers MMM, Olav Sliekers A, Lavik G, Schmid M, Jørgensen BB, Gijs Kuenen J, et al. Anaerobic ammonium oxidation by anammox bacteria in the Black Sea. Nature. 2003;422:608–11.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 13.

    Humbert S, Tarnawski S, Fromin N, Mallet MP, Aragno M, Zopfi J. Molecular detection of anammox bacteria in terrestrial ecosystems: distribution and diversity. ISME J. 2010;4:450–4.

    PubMed 
    Article 

    Google Scholar 

  • 14.

    Zhu GB, Wang SY, Wang Y, Wang CX, Risgaard-Petersen N, Jetten MSM, et al. Anaerobic ammonia oxidation in a fertilized paddy soil. ISME J. 2011;5:1905–12.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 15.

    Oshiki M, Satoh H, Okabe S. Ecology and physiology of anaerobic ammonium oxidizing bacteria. Environ Microbiol. 2016;18:2784–96.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 16.

    Sonthiphand P, Hall MW, Neufeld JD. Biogeography of anaerobic ammonia-oxidizing (anammox) bacteria. Front Microbiol. 2014;5:1–14.

    Article 

    Google Scholar 

  • 17.

    van Bodegom P. Microbial maintenance: A critical review on its quantification. Microb Ecol. 2007;53:513–23.

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 18.

    Wang G, Post WM. A theoretical reassessment of microbial maintenance and implications for microbial ecology modeling. FEMS Microbiol Ecol. 2012;81:610–7.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 19.

    Overkamp W, Ercan O, Herber M, van Maris AJA, Kleerebezem M, Kuipers OP. Physiological and cell morphology adaptation of Bacillus subtilis at near-zero specific growth rates: a transcriptome analysis. Environ Microbiol. 2015;17:346–63.

    PubMed 
    Article 

    Google Scholar 

  • 20.

    Ma X, Wang Y, Zhou S, Yan Y, Lin X, Wu M. Endogenous metabolism of anaerobic ammonium oxidizing bacteria in response to short-term anaerobic and anoxic starvation stress. Chem Eng J. 2017;313:1233–41.

    CAS 
    Article 

    Google Scholar 

  • 21.

    Ma X, Wang Y. Anammox bacteria exhibit capacity to withstand long-term starvation stress: a proteomic-based investigation of survival mechanisms. Chemosphere. 2018;211:952–61.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 22.

    Xing B-S, Guo Q, Jiang X-Y, Chen Q-Q, He M-M, Wu L-M, et al. Long-term starvation and subsequent reactivation of anaerobic ammonium oxidation (anammox) granules. Chem Eng J. 2016;287:575–84.

    CAS 
    Article 

    Google Scholar 

  • 23.

    Wang Q, Song K, Hao X, Wei J, Pijuan M, van Loosdrecht MCM, et al. Evaluating death and activity decay of Anammox bacteria during anaerobic and aerobic starvation. Chemosphere. 2018;201:25–31.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 24.

    Lopez C, Pons MN, Morgenroth E. Endogenous processes during long-term starvation in activated sludge performing enhanced biological phosphorous removal. Water Res. 2006;40:1519–30.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 25.

    Tappe W, Laverman A, Bohland M, Braster M, Rittershaus S, Groeneweg J, et al. Maintenance energy demand and starvation recovery dynamics of Nitrosomonas europaea and Nitrobacter winogradskyi cultivated in a retentostat with complete biomass retention. Appl Environ Microbiol. 1999;65:2471–7.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 26.

    Vos T, Hakkaart XDV, de Hulster EAF, van Maris AJA, Pronk JT, Daran-Lapujade P. Maintenance-energy requirements and robustness of Saccharomyces cerevisiae at aerobic near-zero specific growth rates. Micro Cell Fact. 2016;15:111.

    Article 
    CAS 

    Google Scholar 

  • 27.

    Ali M, Oshiki M, Awata T, Isobe K, Kimura Z, Yoshiaki H, et al. Physiological characterization of anaerobic ammonium oxidizing bacterium “Candidatus Jettenia caeni”. Environ Microbiol. 2015;17:2172–89.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 28.

    Narita Y, Zhang L, Kimura, Ali M, Fujii T, Okabe S. Enrichment and physiological characterization of an anaerobic ammonium-oxidizing bacterium “Candidatus Brocadia sapporoensis”. Syst Appl Microbiol. 2017;40:448–57.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 29.

    Oshiki M, Shimokawa M, Fujii N, Satoh H, Okabe S. Physiological characteristics of the anaerobic ammonium-oxidizing bacterium “Candidatus Brocadia sinica”. Microbiol. 2011;157:1706–13.

    CAS 
    Article 

    Google Scholar 

  • 30.

    Okabe, S, Shafdar, AA, Kobayashi, K, Zhang, L, and Oshiki, M. Glycogen metabolism of the anammox bacterium “Candidatus Brocadia sinica” ISME J. 2020; https://doi.org/10.1038/s41396-020-00850-5.

  • 31.

    van der Star WRL, Miclea AI, van Dongen UGJM, Muyzer G, Picioreanu C, van Loosdrecht MCM. The membrane bioreactor: a novel tool to grow anammox bacteria as free cells. Biotechnol Bioeng. 2008;101:286–94.

    PubMed 
    Article 
    CAS 

    Google Scholar 

  • 32.

    Zhang L, Okabe S. Rapid cultivation of free-living planktonic anammox cells. Water Res. 2017;127:204–10.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 33.

    Oshiki M, Awata T, Kindaichi T, Satoh H, Okabe S. Cultivation of planktonic anaerobic ammonium oxidation (Anammox) bacteria using membrane bioreactor. Microbes Environ. 2013;28:436–43.

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 34.

    Awata T, Oshiki M, Kindaichi T, Ozaki N, Ohashi A, Okabe S. Physiological characterization of an anaerobic ammonium-oxidizing bacterium belonging to the “Candidatus Scalindua” group. Appl Environ Microbiol. 2013;79:4145–8.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 35.

    Zhang L, Narita Y, Gao L, Ali M, Oshiki M, Ishii S, et al. Microbial competition among anammox baxteria in nitrite-limited bioreactors. Water Res. 2017;125:249–58.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 36.

    Graaf AA, Van DE, Bruijn PDE, Robertson LA, Jetten MSM, Kuenen JG. Autotrophic growth of anaerobic in a fluidized bed reactor. Microbiol. 1996;142:2187–96.

    Article 

    Google Scholar 

  • 37.

    Kindaichi T, Awata T, Suzuki Y, Tanabe K, Hatamoto M, Ozaki N, et al. Enrichment using an up-flow column reactor and community structure of marine anammox bacteria from coastal sediment. Microbes Environ. 2011;26:67–73.

    PubMed 
    Article 

    Google Scholar 

  • 38.

    APHA. Standard Methods for the Examination of Water and Sewage, Washington DC,1998,

  • 39.

    Nagaraja P, Shivaswamy M, Kumar H. Highly sensitive N-(1-Naphthyl)ethylene diamine method for the spectrophotometric determination of trace amounts of nitrite in various water samples. Intern J Environ Anal Chem. 2001;80:39–48.

    CAS 
    Article 

    Google Scholar 

  • 40.

    Tsushima I, Ogasawara Y, Kindaichi T, Satoh H, Okabe S. Development of high-rate anaerobic ammonium-oxidizing (anammox) biofilm reactors. Water Res. 2007;41:1623–34.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 41.

    Kindaichi T, Tsushima I, Ogasawara Y, Shimokawa M, Ozaki N, Satoh H, et al. In situ activity and spatial organization of anaerobic ammonium-oxidizing (anammox) bacteria in biofilms. Appl Environ Microbiol. 2007;73:4931–9.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 42.

    Okabe S, Satoh H, Watanabe Y. In situ analysis of nitrifying biofilms as determined by in situ hybridization and the use of microelectrodes. Appl Environ Microbiol. 1999;65:3182–91.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 43.

    Pirt SJ. Maintenance energy of bacteria in growing cultures. Proc R soc Lond B Biol Sci. 1965;163:224–31.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 44.

    Pirt SJ. Maintenance energy: a general model for energy-limited and energy-sufficient growth. Arch Microbiol. 1982;133:300–2.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 45.

    Herbert D, Elsworth R, Telling RC. The continuous culture of bacteria: a theoretical and experimental study. J Gen Microbiol. 1956;14:601–22.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 46.

    van Verseveld HW, De Hollander JA, Frankena J, Braster M, Leeuwerik FJ, Stouthamer AH. Modeling of microbial substrate conversion, growth and product formation in a recycling fermentor. Antonie Van Leeuwenhoek. 1986;52:325–42.

    PubMed 
    Article 

    Google Scholar 

  • 47.

    Lotti T, Kleerebezem R, Lubello C, van Loosdrecht MCM. Physiological and kinetic characterization of a suspended cell anammox culture. Water Res. 2014;60:1–14.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 48.

    Tijhuis L, Van Loosdrecht MCM, Heijnen JJ. A thermodynmically based correlation for maintenance Gibbs energy requirements in aerobic and anaerobic chemotrophic growth. Biotechnol Bioeng. 1993;42:509–19.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 49.

    Strous M, Heijnen JJ, Kuenen JG, Jetten MSM. The sequencing batch reactor as a powerful tool for the study of slowly growing anaerobic ammonium-oxidizing microorganisms. Appl Microbiol Biotechnol. 1998;50:589–96.

    CAS 
    Article 

    Google Scholar 

  • 50.

    Awata T, Kindaichi T, Ozaki N, Ohashi A. Biomass yield efficiency of the marine anammox bacterium, “Candidatus Scalindua sp.,” is affected by salinity. Microbes Environ. 2015;30:86–91.

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 51.

    Henze, M. Wastewater Treatment: Biological and chemical processes. New York, NY: Springer, 1997.

  • 52.

    Vandekerckhove, TGL, Bodé, S, De Mulder, C, Vlaeminck, SE, Boon, N. 13C Incorporation as a tool to estimate biomass yields in thermophilic and mesophilic nitrifying communities. Front Microbiol. 2019;10:192.

  • 53.

    Tappe W, Tomaschewski C, Rittershaus S, Groeneweg J. Cultivation of nitrifying bacteria in the retentostat, a simple fermentor with internal biomass retention. FEMS Microbiol Ecol. 1996;19:47–52.

    CAS 
    Article 

    Google Scholar 

  • 54.

    Rebnegger C, Vos T, Graf AB, Valli M, Pronk JT, Daran-Lapujade P, et al. Picha pastoris exhibits high viability and a low maintenance energy requirement at near-zero specific growth rates. Appl Environ Microbiol. 2016;82:4570–83.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 55.

    Lever MA, Rogers KL, Lloyd KG, Overmann J, Schink B, Thauer RK, et al. Life under extreme energy limitation: a synthesis of laboratory- and field-based investigations. FEMS Microbiol Rev. 2015;39:688–728.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 56.

    Bulthuis BA, Frankena J, Koningstein GM, van Verseveld HW, Stouthamer AH. Instability of protease production in a rel1/rel2 pair of Bacillus licheniformis and associated morphological and physiological characteristics. Antonie Leeuwenhoek. 1988;54:95–111.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 57.

    Kempes, CP, van Bodegom PM, Wolpert, D, Libby, E, Amend, J, Hoehler, T. Drivers of bacterial maintenance and minimal energy requirements. Front Microbiol. 2017;8:31.

  • 58.

    Amend JP, Shock EL. Energetics of overall metabolic reactions of thermophilic and hyperthermophilic Archaea and Bacteria. FEMS Microbiol Rev. 2001;25:175–243.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 59.

    Amend JP, LaRowe DE. Minireview: demystifying microbial reaction energetics. Environ Microbiol. 2019;21:3539–47.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 60.

    Kartal B, Keltjens JT. Anammox biochemistry: a tale of heme c proteins. Trends Biochem Sci. 2016;41:998–1011.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 61.

    Scholten JCM, Conrad R. Energetics of syntrophic propionate oxidation in defined batch and chemostat coculture. Appl Environ Microbiol. 2000;66:2934–42.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 62.

    LaRowe DE, Amend JP. The energetics of anabolism in natural settings. ISME J. 2016;10:1285–95.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 63.

    LaRowe DE, Amend JP. Catabolic rates, population sizes and doubling/replacement times of microorganisms in natural settings. Am J Sci. 2015;315:167–203.

    CAS 
    Article 

    Google Scholar 

  • 64.

    Marschall E, Jogler M, Henssge U, Overmann J. Large-scale distribution and activity patterns of an extremely low-light-adapted population of green sulfur bacteria in the Black Sea. Environ Microbiol. 2010;12:1348–62.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 65.

    Bradley, JA, Arndt, S, Amend, JP, Burwicz, E, Dale, AW, Egger, M et al. Widespread energy limitation to life in global subseafloor sediments. Sci Adv. 2020;6:eaba0697.

  • 66.

    Hoehler TM, Jorgensen BB. Microbial life under extreme energy limitation. Nat Rev Microbiol. 2013;11:83–94.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 67.

    LaRowe, DE, Amend, JP. Power limits for microbial life. Front Microbiol 2015;6:718.

  • 68.

    Zhao R, Mogollon JM, Abby SS, Schleper C, Biddle JF, Roerdink DL. et al. Geochemical transition zone powering microbial growth in subsurface sediments. Proc Natl Acad Sci USA. 2020;117:32617–26.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 69.

    Pitcher A, Villanueva L, Hopmans EC, Schouten S, Reichart G-J, Sinninghe Damste JS. Niche segregation of ammonia-oxidizing archaea and anammox bacteria in the Arabian Sea oxygen minimum zone. ISME J. 2011;5:1896–904.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 70.

    Füssel J, Lam P, Lavik G, Jensen MM, Holtappels M, Günter M, et al. Nitrite oxidation in the Namibian oxygen minimum zone. ISME J. 2012;6:1200–9.

    PubMed 
    Article 
    CAS 

    Google Scholar 

  • 71.

    Füchslin HP, Schneider C, Egli T. In glucose-limited continuous culture the minimum substrate concentration for growth, Smin, is crucial in the competition between the enterobacterium Escherichia coli and Chelatobacter heintzii, an environmentally abundant bacterium. ISME J. 2012;6:777–89.

    PubMed 
    Article 
    CAS 

    Google Scholar 


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