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Intracellular calcite and sulfur dynamics of Achromatium cells observed in a lab-based enrichment and aerobic incubation experiment

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Abstract

We investigated the intracellular dynamics of calcite and sulfur in the large sulfur-oxidizing, calcite-accumulating bacterium Achromatium, with an emphasis on oxygen exposure as a physiological control. For this purpose, morphological changes and possible accretion mechanisms of calcite granules in cells that were freshly collected from natural Achromatium-containing sediment were compared to cells from the same source after prolonged exposure to atmospheric oxygen. Intracellular sulfur is oxidized and removed in response to oxygen exposure. Calcite granules also undergo distinct oxygen-related dynamics; they alternate between tightly packaged, smooth granules with narrow but sharply defined interstitial spaces in atmospheric oxygen-exposed cells, and more loosely packaged granules with irregular, bumpy surface texture and larger interstitial spaces in cells that were not artificially exposed to oxygen. These results suggest that morphological changes of the calcite granules reflect their changing physiological role inside the cell. Sulfur oxidation and calcite dissolution appear to be linked in that proton generation during sulfur oxidation is buffered by gradual calcite erosion, visible in the smooth, rounded surface morphology observed after oxygen exposure. Our results support the hypothesis that calcite dynamics buffer the intracellular pH fluctuations linked to electron acceptor limitation during proton-consuming sulfide oxidation to sulfur, and electron acceptor abundance during proton-generating sulfur oxidation to sulfate.

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References

  • Babenzien HD (1991) Achromatium oxaliferum and its ecological niche. Zentralbl Mikrobiol 146:41–49

    Article  Google Scholar 

  • Cossy J, Pale P (1987) Silylation selective par L’Hexamethyldisilazane. Tetrahedron Lett 28:6039–6040

    Article  CAS  Google Scholar 

  • Erdogan M (2000) Measurement of polished rock surface brightness by image analysis method. Eng Geol 57:65–72

    Article  Google Scholar 

  • Glöckner FO, Babenzien HD, Wulf J, Amann R (1999) Phylogeny and diversity of Achromatium oxaliferum. Syst Appl Microbiol 22:28–38

    Article  PubMed  Google Scholar 

  • Gray ND (2006) The unique role of intracellular calcification in the genus Achromatium. In: Shiverly JM (ed) Inclusions in Prokaryotes. Microbiol. Monographs 1. Springer, Berlin, pp 299–309

    Chapter  Google Scholar 

  • Gray ND, Head IM (2014) The family Achromatiaceae. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson FL (eds) The Prokaryotes: Gammaproteobacteria. Springer, Berlin, pp 1–14

    Google Scholar 

  • Gray ND, Pickup RW, Jones JG, Head IM (1997) Ecophysiological evidence that Achromatium oxaliferum is responsible for the oxidation of reduced sulfur species to sulfate in a freshwater sediment. Appl Environ Microbiol 63:1905–1910

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gray ND, Howarth R, Pickup RW, Gwyn Jones J, Head IM (1999) Substrate uptake by uncultured bacteria from the genus Achromatium determined by microautoradiography. Appl Environ Microbiol 65:5100–5106

    CAS  PubMed  PubMed Central  Google Scholar 

  • Head IM, Gray ND, Clarke KJ, Pickup RW, Jones JG (1996) The phylogenetic position and ultrastructure of the uncultured bacterium Achromatium oxaliferum. Microbiology 142:2341–2354

    Article  CAS  PubMed  Google Scholar 

  • Head IM, Gray ND, Howarth R, Pickup RW, Clarke KJ, Jones JG (2000) Achromatium oxaliferum—understanding the unmistakable. In: Schink B (ed) Advances in Microbial Ecology, vol 16. Kluwer Academic/Plenum Publishers, New York, pp 1–40

    Chapter  Google Scholar 

  • Ionescu D, Bizic-Ionescu M, De Maio N, Cypionka H, Grossart HP (2017) Community-like genome in single cells of the sulfur bacterium Achromatium oxaliferum. Nat Commun 8:455. https://doi.org/10.1038/s41467-017-00342-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • La Rivière JWM, Schmidt K (1992) Morphologically conspicuous sulfur-oxidizing Eubacteria. In: Trüper HG, Dworkin M, Harder W, Schleifer KH, Balows A (eds) The Prokaryotes. Springer, New York, pp 3934–3947

    Chapter  Google Scholar 

  • Lauterborn H (1915) Die sapropelische Lebewelt. Ein Beitrag zur Biologie des Faulschlamms natürlicher Gewässer. Verhandl Naturhistor Mediz Ver Heidelberg 13:395–481

    Google Scholar 

  • Mansor M, Hamilton TL, Fantle MS, Macalady J (2015) Metabolic diversity and ecological niches of Achromatium populations revealed with single-cell genomic sequencing. Front Microbiol 6:822. https://doi.org/10.3389/fmicb.2015.00822

    Article  PubMed  PubMed Central  Google Scholar 

  • Pellegata R, Pinza M, Pifferi G (1978) An improved synthesis of γ-, δ-, and ε-Lactams. Synthesis 8:614–616

    Article  Google Scholar 

  • Salman V, Yang T, Berben T, Klein F, Angert E, Teske A (2015) Calcite-accumulating large sulfur bacteria of the genus Achromatium in Sippewissett Salt Marsh. ISME J 9:2503–2514

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Salman V, Berben T, Bowers RM, Wojke T, Teske A, Angert E (2016) Insights into the single cell draft genome of Candidatus “Achromatium palustre”. Stand Genom Sci 11:28. https://doi.org/10.1186/s40793-016-0146-x

    Article  CAS  Google Scholar 

  • Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schorn S, Cypionka H (2018) A crispy diet: grazers of Achromatium oxaliferum in Lake Stechlin Sediments. Microbial Ecology. https://doi.org/10.1007/s00248-018-1158-4. [Epub ahead of print]

  • Seitz AP, Nielsen TH, Overmann J (1993) Physiology of purple sulfur bacteria forming macroscopic aggregates in Great Sippewissett salt marsh, Massachusetts. FEMS Microbiol Ecol 12:225–236

    Article  CAS  Google Scholar 

  • Steudel R (2003) Aqueous Sulfur Sols. Top Curr Chem 230:153–166

    Article  CAS  Google Scholar 

  • West GS, Griffiths BM (1913) The lime-sulphur bacteria of the genus Hillhousia. Ann Bot 27:83–91

    Article  Google Scholar 

  • Wilbanks EG, Jaekel U, Salman V, Humphrey PT, Eisen JA, Facciotti MT, Buckley DH, Zinder SH, Gruschel GK, Fike DA, Orphan VJ (2014) A sulfurous symbiosis: microscale sulfur cycling in the pink berry consortia of the Sippewissett salt marsh. Environ Microbiol 16:3398–3415

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This study was initiated during the 2013 Microbial Diversity Course, Marine Biological Laboratory, Woods Hole, MA. We thank the course directors, Dr. Dan Buckley and Dr. Steve Zinder, as well as all assistants for their tremendous support. TY received the Horace W. Stunkard Scholarship and a post-course fellowship from MBL, and was supported further by a visiting student fellowship at Aarhus University to perform the microelectrode measurements. We thank Lars Borregaard Pedersen and Preben Grann Sørensen for their great help in the microsensor lab at Aarhus University. We also thank Dr. Virginia Edgcomb from Woods Hole Oceanographic Institution for her tremendous help on sampling.

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Authors and Affiliations

  1. Department of Marine Sciences, University of North Carolina at Chapel Hill, Chapel Hill, USA

    Tingting Yang & Andreas Teske

  2. Department of Applied Physical Sciences, University of North Carolina at Chapel Hill, Chapel Hill, USA

    Wallace Ambrose

  3. HGF MPG Joint Research Group for Deep-Sea Ecology and Technology, Max Planck Institute for Marine Microbiology, Bremen, Germany

    Verena Salman-Carvalho

  4. Microscopy Services Laboratory, University of North Carolina at Chapel Hill, Chapel Hill, USA

    Robert Bagnell

  5. Department of Bioscience, Center for Geomicrobiology, Aarhus, Denmark

    Tingting Yang & Lars Peter Nielsen

Authors
  1. Tingting Yang
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  2. Andreas Teske
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  3. Wallace Ambrose
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  4. Verena Salman-Carvalho
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  5. Robert Bagnell
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  6. Lars Peter Nielsen
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Contributions

TY took samples, did SEM–EDS, analysed data and wrote the first versions of the manuscript. AT assisted with the incubation experiment, revised the manuscript, and provided advice on data interpretation. WA helped with SEM–EDS, performed FIB, and provided suggestions. RB worked on overnight cell observation and provided good method suggestions. VS-C assisted with fieldwork, provided advice on data interpretation, and revised the manuscript. LPN mentored the microelectrode experiment.

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Correspondence to Tingting Yang.

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Yang, T., Teske, A., Ambrose, W. et al. Intracellular calcite and sulfur dynamics of Achromatium cells observed in a lab-based enrichment and aerobic incubation experiment. Antonie van Leeuwenhoek 112, 263–274 (2019). https://doi.org/10.1007/s10482-018-1153-2

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  • DOI: https://doi.org/10.1007/s10482-018-1153-2

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