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

  • Tingting Yang
  • Andreas Teske
  • Wallace Ambrose
  • Verena Salman-Carvalho
  • Robert Bagnell
  • Lars Peter Nielsen
Original Paper

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.

Keywords

Achromatium Geomicrobiology Intracellular calcite granules Redox Sulfur-oxidizing bacteria 

Notes

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.

Authors’ 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.

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10482_2018_1153_MOESM1_ESM.mov (208.7 mb)
Supplementary material 1 (MOV 213683 kb)
10482_2018_1153_MOESM2_ESM.docx (3.9 mb)
Supplementary material 2 (DOCX 4009 kb)

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Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.Department of Marine SciencesUniversity of North Carolina at Chapel HillChapel HillUSA
  2. 2.Department of Applied Physical SciencesUniversity of North Carolina at Chapel HillChapel HillUSA
  3. 3.HGF MPG Joint Research Group for Deep-Sea Ecology and TechnologyMax Planck Institute for Marine MicrobiologyBremenGermany
  4. 4.Microscopy Services LaboratoryUniversity of North Carolina at Chapel HillChapel HillUSA
  5. 5.Department of BioscienceCenter for GeomicrobiologyAarhusDenmark

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