Abstract
Large sulfur bacteria of the genus Achromatium are exceptional among Bacteria and Archaea as they can accumulate high amounts of internal calcite. Although known for more than 100 years, they remain uncultured, and only freshwater populations have been studied so far. Here we investigate a marine population of calcite-accumulating bacteria that is primarily found at the sediment surface of tide pools in a salt marsh, where high sulfide concentrations meet oversaturated oxygen concentrations during the day. Dynamic sulfur cycling by phototrophic sulfide-oxidizing and heterotrophic sulfate-reducing bacteria co-occurring in these sediments creates a highly sulfidic environment that we propose induces behavioral differences in the Achromatium population compared with reported migration patterns in a low-sulfide environment. Fluctuating intracellular calcium/sulfur ratios at different depths and times of day indicate a biochemical reaction of the salt marsh Achromatium to diurnal changes in sedimentary redox conditions. We correlate this calcite dynamic with new evidence regarding its formation/mobilization and suggest general implications as well as a possible biological function of calcite accumulation in large bacteria in the sediment environment that is governed by gradients. Finally, we propose a new taxonomic classification of the salt marsh Achromatium based on their adaptation to a significantly different habitat than their freshwater relatives, as indicated by their differential behavior as well as phylogenetic distance on 16S ribosomal RNA gene level. In future studies, whole-genome characterization and additional ecophysiological factors could further support the distinctive position of salt marsh Achromatium.
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Acknowledgements
Much of this work was performed during several MBL Microbial Diversity summer courses. We warmly thank the course directors, Dan Buckley, Steve Zinder, Dianne Newman and Jared Leadbetter, as well as all course associates for the outstanding opportunity and support. Research at MBL was funded by the Howard Hughes Medical Foundation, the Simons Foundation, the Gordon and Betty Moore Foundation (2493), the National Science Foundation (DEB-0917499), the US Department of Energy (DE-FG02-10ER13361), the NASA Astrobiology Institute and the Beckman Foundation. In addition, we thank the Borisy lab at MBL, Ginny Edgcomb at WHOI and Becky Williams and Kit Umbach at Cornell University for lab space and technical support. Finally, we thank the editor and reviewers for their contribution to greatly improve this manuscript. VS is supported by the Deutsche Forschungsgemeinschaft (Sa 2505/1-1), TB by the ERC advanced Grant PARASOL (No. 322551), and TY received financial assistance at the MBL from the Horace W Stunkard Scholarship Fund.
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Salman, V., Yang, T., Berben, T. et al. Calcite-accumulating large sulfur bacteria of the genus Achromatium in Sippewissett Salt Marsh. ISME J 9, 2503–2514 (2015). https://doi.org/10.1038/ismej.2015.62
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DOI: https://doi.org/10.1038/ismej.2015.62
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