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Intracellular amorphous Ca-carbonate and magnetite biomineralization by a magnetotactic bacterium affiliated to the Alphaproteobacteria

  • 1.

    Weiner S, Dove PM. An overview of biomineralization processes and the problem of the vital effect. Rev Miner Geochem. 2003;54:1–29.

    CAS  Google Scholar 

  • 2.

    Benzerara K, Miot J, Morin G, Ona-Nguema G, Skouri-Panet F, Férard C. Significance, mechanisms and environmental implications of microbial biomineralization. Comptes Rendus Geosci. 2011;343:160–7.

    CAS  Google Scholar 

  • 3.

    Lowenstam HA. Minerals formed by organisms. Science. 1981;211:1126–31.

    CAS  PubMed  Google Scholar 

  • 4.

    Blakemore R. Magnetotactic bacteria. Science. 1975;190:377–9.

    CAS  PubMed  Google Scholar 

  • 5.

    Uebe R, Schüler D. Magnetosome biogenesis in magnetotactic bacteria. Nat Rev Microbiol. 2016;14:621–37.

    CAS  PubMed  Google Scholar 

  • 6.

    Grant CR, Wan J, Komeili A. Organelle formation in bacteria and archaea. Annu Rev Cell Dev Biol. 2018;34:217–38.

    CAS  PubMed  Google Scholar 

  • 7.

    Schewiakoff W. Über einen neuen bacterienahnlichen organismus des Süsswassers. Heidelb Habilit. 1893;1–38.

  • 8.

    West GS, Griffiths BM. The lime-sulphur bacteria of the genus hillhousia. Ann Bot. 1913;os-27:83–91.

    Google Scholar 

  • 9.

    Head IM, Gray ND, Clarke KJ, Pickup RW, Jones JG. The phylogenetic position and ultrastructure of the uncultured bacterium Achromatium oxaliferum. Microbiol Read Engl. 1996;142(Pt 9):2341–54.

    CAS  Google Scholar 

  • 10.

    Salman V, Yang T, Berben T, Klein F, Angert E, Teske A. Calcite-accumulating large sulfur bacteria of the genus Achromatium in Sippewissett Salt Marsh. ISME J. 2015;9:2503–14.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 11.

    Mansor M, Hamilton TL, Fantle MS, Macalady J. Metabolic diversity and ecological niches of Achromatium populations revealed with single-cell genomic sequencing. Front Microbiol. 2015;6:822.

    PubMed  PubMed Central  Google Scholar 

  • 12.

    Gray N, Head I. The family achromatiaceae. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F, editors. The Prokaryotes: Gammaproteobacteria. Berlin, Heidelberg: Springer; 2014. p. 1–14.

  • 13.

    Head IM, Gray ND, Howarth R, Pickup RW, Clarke KJ, Jones JG. Achromatium oxaliferum Understanding the Unmistakable. In: Schink B, editor. Advances in microbial ecology. Boston, MA: Springer US; 2000. p. 1–40.

  • 14.

    Babenzien H-D, Sass H. The sediment-water interface—habitat of the unusual bacterium Achromatium oxaliferum. Adv Limnol. 1996;48:247–51.

    Google Scholar 

  • 15.

    Gray ND, Pickup RW, Jones JG, Head IM. Ecophysiological evidence that achromatium oxaliferum is responsible for the oxidation of reduced sulfur species to sulfate in a freshwater sediment. Appl Environ Microbiol. 1997;63:1905–10.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 16.

    Gray ND, Howarth R, Pickup RW, Jones JG, Head IM. Substrate uptake by uncultured bacteria from the genus Achromatium determined by microautoradiography. Appl Environ Microbiol. 1999;65:5100–6.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 17.

    Babenzien H-D. Achromatium oxaliferum and its ecological niche. Zentralblatt Für Mikrobiol. 1991;146:41–49.

    Google Scholar 

  • 18.

    Gray ND, Comaskey D, Miskin IP, Pickup RW, Suzuki K, Head IM. Adaptation of sympatric Achromatium spp. to different redox conditions as a mechanism for coexistence of functionally similar sulphur bacteria. Environ Microbiol. 2004;6:669–77.

    CAS  PubMed  Google Scholar 

  • 19.

    Couradeau E, Benzerara K, Gérard E, Moreira D, Bernard S, Brown GE, et al. An early-branching microbialite cyanobacterium forms intracellular carbonates. Science. 2012;336:459–62.

    CAS  PubMed  Google Scholar 

  • 20.

    Cam N, Benzerara K, Georgelin T, Jaber M, Lambert J-F, Poinsot M, et al. Selective Uptake of Alkaline Earth Metals by Cyanobacteria Forming Intracellular Carbonates. Environ Sci Technol. 2016;50:11654–62.

    CAS  PubMed  Google Scholar 

  • 21.

    Blondeau M, Sachse M, Boulogne C, Gillet C, Guigner J-M, Skouri-Panet F, et al. Amorphous calcium carbonate granules form within an intracellular compartment in calcifying cyanobacteria. Front Microbiol. 2018;9:1768.

    PubMed  PubMed Central  Google Scholar 

  • 22.

    Li J, Margaret Oliver I, Cam N, Boudier T, Blondeau M, Leroy E, et al. Biomineralization patterns of intracellular carbonatogenesis in cyanobacteria: molecular hypotheses. Minerals. 2016;6:10.

  • 23.

    Benzerara K, Skouri-Panet F, Li J, Férard C, Gugger M, Laurent T, et al. Intracellular Ca-carbonate biomineralization is widespread in cyanobacteria. Proc Natl Acad Sci USA. 2014;111:10933–8.

    CAS  PubMed  Google Scholar 

  • 24.

    Bradley JA, Daille LK, Trivedi CB, Bojanowski CL, Stamps BW, Stevenson BS, et al. Carbonate-rich dendrolitic cones: insights into a modern analog for incipient microbialite formation, Little Hot Creek, Long Valley Caldera, California. NPJ Biofilms Microbiomes. 2017;3:32.

    PubMed  PubMed Central  Google Scholar 

  • 25.

    Moreira D, Tavera R, Benzerara K, Skouri-Panet F, Couradeau E, Gérard E, et al. Description of Gloeomargarita lithophora gen. nov., sp. nov., a thylakoid-bearing, basal-branching cyanobacterium with intracellular carbonates, and proposal for Gloeomargaritales ord. nov. Int J Syst Evol Microbiol. 2017;67:653–8.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 26.

    Mehta N, Benzerara K, Kocar BD, Chapon V. Sequestration of radionuclides radium-226 and strontium-90 by cyanobacteria forming intracellular calcium carbonates. Environ Sci Technol. 2019;53:12639–47.

    CAS  PubMed  Google Scholar 

  • 27.

    Ponce-Toledo RI, Deschamps P, López-García P, Zivanovic Y, Benzerara K, Moreira D. An early-branching freshwater cyanobacterium at the origin of plastids. Curr Biol CB. 2017;27:386–91.

    CAS  PubMed  Google Scholar 

  • 28.

    la Rivière JWM, Schmidt K. Morphologically Conspicuous Sulfur-Oxidizing Eubacteria. In: Starr MP, Stolp H, Trüper HG, Balows A, Schlegel HG, editors. The prokaryotes: a handbook on habitats, isolation, and identification of bacteria. Berlin Heidelberg: Springer; 1981. p. 1037–48.

  • 29.

    Gray ND. The unique role of intracellular calcification in the genus achromatium. In: Shively JM, editor. Inclusions in prokaryotes. Berlin, Heidelberg: Springer; 2006. p. 299–309.

  • 30.

    Miot J, Jezequel D, Benzerara K, Cordier L, Rivas-Lamelo S, Skouri-Panet F, et al. Mineralogical diversity in lake pavin: connections with water column chemistry and biomineralization processes. Minerals. 2016;6:UNSP 24.

    Google Scholar 

  • 31.

    Podda F, Michard G. Mesure colorimétrique de l’alcalinité. Comptes Rendus Acad Sci – Sér II. 1994;319:651–7.

    CAS  Google Scholar 

  • 32.

    Sarazin G, Michard G, Prevot F. A rapid and accurate spectroscopic method for alkalinity measurements in sea water samples. Water Res. 1999;33:290–4.

    CAS  Google Scholar 

  • 33.

    Zeyen N, Daval D, Lopez-Garcia P, Moreira D, Gaillardet J, Benzerara K. Geochemical conditions allowing the formation of modern lacustrine microbialites. Procedia Earth Planet Sci. 2017;17:380–3.

    Google Scholar 

  • 34.

    Purgstaller B, Goetschl KE, Mavromatis V, Dietzel M. Solubility investigations in the amorphous calcium magnesium carbonate system. CrystEngComm. 2018;21:155–64.

    PubMed  PubMed Central  Google Scholar 

  • 35.

    Schüler D. The biomineralization of magnetosomes in Magnetospirillum gryphiswaldense. Int Microbiol J Span Soc Microbiol. 2002;5:209–14.

    Google Scholar 

  • 36.

    Lane DJ. 16S/23S sequencing. In: Stackebrandt E, Goodfellow M, editor. Nucleic acid techniques in bacterial systematics. New York: John Wiley & Sons; 1991. p. 115–75.

  • 37.

    Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, Miller W, et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997;25:3389–402.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 38.

    Edgar RC. UCHIME2: improved chimera prediction for amplicon sequencing. bioRxiv 2016. https://www.biorxiv.org/content/10.1101/074252v1.

  • 39.

    Gascuel O. BIONJ: an improved version of the NJ algorithm based on a simple model of sequence data. Mol Biol Evol. 1997;14:685–95.

    CAS  PubMed  Google Scholar 

  • 40.

    Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013;30:772–80.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 41.

    Talavera G, Castresana J. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol. 2007;56:564–77.

    CAS  PubMed  Google Scholar 

  • 42.

    Nguyen L-T, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol. 2015;32:268–74.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 43.

    Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods. 2017;14:587–9.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 44.

    Pernthaler J, Glockner FO, Schonhuber W, Amann R. Fluorescence in situ hybridization (FISH) with rRNA-targeted oligonucleotide probes. Methods Microbiol Vol 30. 2001;30:207–26.

    CAS  Google Scholar 

  • 45.

    Cole JR, Chai B, Marsh TL, Farris RJ, Wang Q, Kulam SA, et al. The Ribosomal Database Project (RDP-II): previewing a new autoaligner that allows regular updates and the new prokaryotic taxonomy. Nucleic Acids Res. 2003;31:442–3.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 46.

    Rivas-Lamelo S, Benzerara K, Lefèvre CT, Jézéquel D, Menguy N, Viollier E, et al. Magnetotactic bacteria as a new model for P sequestration in the ferruginous Lake Pavin. Geochem Perspect Lett. 2017;5:35–41.

    Google Scholar 

  • 47.

    Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinforma Oxf Engl. 2014;30:2114–20.

    CAS  Google Scholar 

  • 48.

    Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics. 2014;30:2068–9.

    CAS  PubMed  Google Scholar 

  • 49.

    Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 2015;25:1043–55.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 50.

    Belkhou R, Stanescu S, Swaraj S, Besson A, Ledoux M, Hajlaoui M, et al. HERMES: a soft X-ray beamline dedicated to X-ray microscopy. J Synchrotron Radiat. 2015;22:968–79.

    PubMed  Google Scholar 

  • 51.

    Swaraj S, Belkhou R, Stanescu S, Rioult M, Besson A, Hitchcock AP. Performance of the HERMES beamline at the carbon K-edge. J Phys Conf Ser. 2017;849:012046.

    Google Scholar 

  • 52.

    Le Nagard L, Zhu X, Yuan H, Benzerara K, Bazylinski DA, Fradin C, et al. Magnetite magnetosome biomineralization in Magnetospirillum magneticum strain AMB-1: A time course study. Chem Geol. 2019;530:119348.

    Google Scholar 

  • 53.

    Cosmidis J, Benzerara K. Soft x-ray scanning transmission spectro-microscopy. In: Elaine DiMasi, Laurie B. Gower, editors. Biomineralization sourcebook: characterization of biominerals and biomimetic materials. CRC Press; 2014.

  • 54.

    Lefèvre CT. Genomic insights into the early-diverging magnetotactic bacteria. Environ Microbiol. 2016;18:1–3.

    PubMed  Google Scholar 

  • 55.

    Benzerara K, Yoon TH, Tyliszczak T, Constantz B, Spormann AM, Brown GE. Scanning transmission X-ray microscopy study of microbial calcification. Geobiology. 2004;2:249–59.

    Google Scholar 

  • 56.

    Michard G, Viollier E, Jézéquel D, Sarazin G. Geochemical study of a crater lake: Pavin Lake, France — Identification, location and quantification of the chemical reactions in the lake. Chem Geol. 1994;115:103–15.

    CAS  Google Scholar 

  • 57.

    Konstantinidis KT, Rosselló-Móra R, Amann R. Uncultivated microbes in need of their own taxonomy. ISME J. 2017;11:2399–406.

    PubMed  PubMed Central  Google Scholar 

  • 58.

    Cai H, Wang Y, Xu H, Yan Z, Jia B, Majid Maszenan A, et al. Niveispirillum cyanobacteriorum sp. nov., a nitrogen-fixing bacterium isolated from cyanobacterial aggregates in a eutrophic lake. Int J Syst Evol Microbiol. 2015;65:2537–41.

    CAS  PubMed  Google Scholar 

  • 59.

    Zhang D, Yang H, Zhang W, Huang Z, Liu S-J. Rhodocista pekingensis sp. nov., a cyst-forming phototrophic bacterium from a municipal wastewater treatment plant. Int J Syst Evol Microbiol. 2003;53:1111–4.

    CAS  PubMed  Google Scholar 

  • 60.

    Chung EJ, Park TS, Kim KH, Jeon CO, Lee H-I, Chang W-S, et al. Nitrospirillum irinus sp. nov., a diazotrophic bacterium isolated from the rhizosphere soil of Iris and emended description of the genus Nitrospirillum. Antonie Van Leeuwenhoek. 2015;108:721–9.

    CAS  PubMed  Google Scholar 

  • 61.

    Bashan Y, Holguin G, de-Bashan LE. Azospirillum-plant relationships: physiological, molecular, agricultural, and environmental advances (1997-2003). Can J Microbiol. 2004;50:521–77.

    CAS  PubMed  Google Scholar 

  • 62.

    Guo Q, Zhou Z, Zhang L, Zhang C, Chen M, Wang B, et al. Skermanella pratensis sp. nov., isolated from meadow soil, and emended description of the genus Skermanella. Int J Syst Evol Microbiol. 2020;70:1605–9.

    PubMed  Google Scholar 

  • 63.

    Lefèvre CT, Bazylinski DA. Ecology, diversity, and evolution of magnetotactic bacteria. Microbiol Mol Biol Rev. 2013;77:497–526.

    PubMed  PubMed Central  Google Scholar 

  • 64.

    Lin W, Bazylinski DA, Xiao T, Wu L-F, Pan Y. Life with compass: diversity and biogeography of magnetotactic bacteria. Environ Microbiol. 2014;16:2646–58.

    CAS  PubMed  Google Scholar 

  • 65.

    Bazylinski DA, Dean AJ, Williams TJ, Long LK, Middleton SL, Dubbels BL. Chemolithoautotrophy in the marine, magnetotactic bacterial strains MV-1 and MV-2. Arch Microbiol. 2004;182:373–87.

    CAS  PubMed  Google Scholar 

  • 66.

    Schultheiss D, Handrick R, Jendrossek D, Hanzlik M, Schüler D. The presumptive magnetosome protein Mms16 is a poly(3-hydroxybutyrate) granule-bound protein (phasin) in Magnetospirillum gryphiswaldense. J Bacteriol. 2005;187:2416–25.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 67.

    Lefèvre CT, Bernadac A, Yu-Zhang K, Pradel N, Wu L-F. Isolation and characterization of a magnetotactic bacterial culture from the Mediterranean Sea. Environ Microbiol. 2009;11:1646–57.

    PubMed  Google Scholar 

  • 68.

    Qian X-X, Liu J, Menguy N, Li J, Alberto F, Teng Z, et al. Identification of novel species of marine magnetotactic bacteria affiliated with Nitrospirae phylum. Environ Microbiol Rep. 2019;11:330–7.

    CAS  PubMed  Google Scholar 

  • 69.

    Lefèvre CT, Frankel RB, Abreu F, Lins U, Bazylinski DA. Culture-independent characterization of a novel, uncultivated magnetotactic member of the Nitrospirae phylum. Environ Microbiol. 2011;13:538–49.

    PubMed  Google Scholar 

  • 70.

    Cox BL, Popa R, Bazylinski DA, Lanoil B, Douglas S, Belz A, et al. Organization and elemental analysis of P-, S-, and Fe-rich inclusions in a population of freshwater magnetococci. Geomicrobiol J. 2002;19:387–406.

    CAS  Google Scholar 

  • 71.

    Byrne ME, Ball DA, Guerquin-Kern J-L, Rouiller I, Wu T-D, Downing KH, et al. Desulfovibrio magneticus RS-1 contains an iron- and phosphorus-rich organelle distinct from its bullet-shaped magnetosomes. Proc Natl Acad Sci USA. 2010;107:12263–8.

    CAS  PubMed  Google Scholar 

  • 72.

    Keim CN, Solórzano G, Farina M, Lins U. Intracellular inclusions of uncultured magnetotactic bacteria. Int Microbiol J Span Soc Microbiol. 2005;8:111–7.

    CAS  Google Scholar 

  • 73.

    Schulz-Vogt HN, Pollehne F, Jürgens K, Arz HW, Beier S, Bahlo R, et al. Effect of large magnetotactic bacteria with polyphosphate inclusions on the phosphate profile of the suboxic zone in the Black Sea. ISME J. 2019;13:1198–208.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 74.

    Blondeau M, Benzerara K, Ferard C, Guigner J-M, Poinsot M, Coutaud M, et al. Impact of the cyanobacterium Gloeomargarita lithophora on the geochemical cycles of Sr and Ba. Chem Geol. 2018;483:88–97.

    CAS  Google Scholar 

  • 75.

    Anbu P, Kang C-H, Shin Y-J, So J-S. Formations of calcium carbonate minerals by bacteria and its multiple applications. Springerplus. 2016;5:250.

    PubMed  PubMed Central  Google Scholar 

  • 76.

    Cam N, Benzerara K, Georgelin T, Jaber M, Lambert J-F, Poinsot M, et al. Cyanobacterial formation of intracellular Ca-carbonates in undersaturated solutions. Geobiology. 2018;16:49–61.

    CAS  PubMed  Google Scholar 

  • 77.

    Toro-Nahuelpan M, Müller FD, Klumpp S, Plitzko JM, Bramkamp M, Schüler D. Segregation of prokaryotic magnetosomes organelles is driven by treadmilling of a dynamic actin-like MamK filament. BMC Biol. 2016;14:88.

    PubMed  PubMed Central  Google Scholar 

  • 78.

    Toro-Nahuelpan M, Giacomelli G, Raschdorf O, Borg S, Plitzko JM, Bramkamp M, et al. MamY is a membrane-bound protein that aligns magnetosomes and the motility axis of helical magnetotactic bacteria. Nat Microbiol. 2019;4:1978–89.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 79.

    Lefèvre CT, Bennet M, Klumpp S, Faivre D. Positioning the flagellum at the center of a dividing cell to combine bacterial division with magnetic polarity. mBio. 2015;6:e02286.

    PubMed  PubMed Central  Google Scholar 

  • 80.

    Judd EM, Ryan KR, Moerner WE, Shapiro L, McAdams HH. Fluorescence bleaching reveals asymmetric compartment formation prior to cell division in Caulobacter. Proc Natl Acad Sci USA. 2003;100:8235–40.

    CAS  PubMed  Google Scholar 

  • 81.

    Klumpp S, Lefèvre CT, Bennet M, Faivre D. Swimming with magnets: From biological organisms to synthetic devices. Phys Rep. 2019;789:1–54.

    Google Scholar 

  • 82.

    Lefèvre CT, Abreu F, Lins U, Bazylinski DA. Nonmagnetotactic multicellular prokaryotes from low-saline, nonmarine aquatic environments and their unusual negative phototactic behavior. Appl Environ Microbiol. 2010;76:3220–7.

    PubMed  PubMed Central  Google Scholar 

  • 83.

    Walsby AE. Gas vesicles. Microbiol Rev. 1994;58:94–144.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 84.

    Walsby A. The properties and buoyancy-providing role of gas vacuoles in trichodesmium ehrenberg. Br Phycol J. 1978;13:103–16.

    Google Scholar 

  • 85.

    Monteil CL, Menguy N, Prévéral S, Warren A, Pignol D, Lefèvre CT. Accumulation and dissolution of magnetite crystals in a magnetically responsive ciliate. Appl Environ Microbiol. 2018;84:e02865-17.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 86.

    Monteil CL, Vallenet D, Menguy N, Benzerara K, Barbe V, Fouteau S, et al. Ectosymbiotic bacteria at the origin of magnetoreception in a marine protist. Nat Microbiol. 2019;4:1088–95.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 87.

    Leão P, Nagard LL, Yuan H, Cypriano J, Silva‐Neto ID, Bazylinski DA, et al. Magnetosome magnetite biomineralization in a flagellated protist: evidence for an early evolutionary origin for magnetoreception in eukaryotes. Environ Microbiol. 2020;22:1495–506.

    PubMed  Google Scholar 

  • 88.

    Isambert A, Menguy N, Larquet E, Guyot F, Valet J-P. Transmission electron microscopy study of magnetites in a freshwater population of magnetotactic bacteria. Am Miner. 2007;92:621–30.

    CAS  Google Scholar 

  • 89.

    Taoka A, Kondo J, Oestreicher Z, Fukumori Y. Characterization of uncultured giant rod-shaped magnetotactic Gammaproteobacteria from a freshwater pond in Kanazawa, Japan. Microbiol Read Engl. 2014;160:2226–34.

    CAS  Google Scholar 

  • 90.

    Monteil CL, Perrière G, Menguy N, Ginet N, Alonso B, Waisbord N, et al. Genomic study of a novel magnetotactic Alphaproteobacteria uncovers the multiple ancestry of magnetotaxis. Environ Microbiol. 2018;20:4415–30.

    CAS  PubMed  Google Scholar 


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