Frontiers of Earth Science

, Volume 12, Issue 1, pp 160–169 | Cite as

Live microbial cells adsorb Mg2+ more effectively than lifeless organic matter

Research Article

Abstract

The Mg2+ content is essential in determining different Mg-CaCO3 minerals. It has been demonstrated that both microbes and the organic matter secreted by microbes are capable of allocating Mg2+ and Ca2+ during the formation of Mg-CaCO3, yet detailed scenarios remain unclear. To investigate the mechanism that microbes and microbial organic matter potentially use to mediate the allocation of Mg2+ and Ca2+ in inoculating systems, microbial mats and four marine bacterial strains (Synechococcus elongatus, Staphylococcus sp., Bacillus sp., and Desulfovibrio vulgaris) were incubated in artificial seawater media with Mg/Ca ratios ranging from 0.5 to 10.0. At the end of the incubation, the morphology of the microbial mats and the elements adsorbed on them were analyzed using scanning electronic microscopy (SEM) and energy diffraction spectra (EDS), respectively. The content of Mg2+ and Ca2+ adsorbed by the extracellular polysaccharide substances (EPS) and cells of the bacterial strains were analyzed with atomic adsorption spectroscopy (AAS). The functional groups on the surface of the cells and EPS of S. elongatus were estimated using automatic potentiometric titration combined with a chemical equilibrium model. The results show that live microbial mats generally adsorb larger amounts of Mg2+ than Ca2+, while this rarely is the case for autoclaved microbial mats. A similar phenomenon was also observed for the bacterial strains. The living cells adsorb more Mg2+ than Ca2+, yet a reversed trend was observed for EPS. The functional group analysis indicates that the cell surface of S. elongatus contains more basic functional groups (87.24%), while the EPS has more acidic and neutral functional groups (83.08%). These features may be responsible for the different adsorption behavior of Mg2+ and Ca2+ by microbial cells and EPS. Our work confirms the differential Mg2+ and Ca2+ mediation by microbial cells and EPS, which may provide insight into the processes that microbes use to induce Mg-carbonate formation.

Keywords

microbe adsorption magnesium calcium 

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Notes

Acknowledgements

We greatly thank Man Lu for her help with the titration work. This study was jointly supported by the National Natural Science Foundation of China (Grant Nos. 41130207 and 41502317), the Special Funds for Basic Scientific Research of Central Colleges, China University of Geosciences (Wuhan) (CUG120103), and the open research program from the State Key Laboratory of Biogeology and Environmental Biology (GBL21503).

References

  1. Acuña N, Ortega-Morales B O, Valadez-González A (2006). Biofilm colonization dynamics and its influence on the corrosion resistance of austenitic UNS S31603 stainless steel exposed to Gulf of Mexico seawater. Mar Biotechnol (NY), 8(1): 62–70CrossRefGoogle Scholar
  2. Baker P A, Burns S J (1985). Occurrence and formation of dolomite in organic-rich continental margin sediments. AAPG Bull, 69(11): 1917–1930Google Scholar
  3. Beveridge T, Murray R (1980). Sites of metal deposition in the cell wall of Bacillus subtilis. J Bacteriol, 141(2): 876–887Google Scholar
  4. Bontognali T R, McKenzie J A, Warthmann R J, Vasconcelos C (2014). Microbially influenced formation of Mg-calcite and Ca-dolomite in the presence of exopolymeric substances produced by sulphatereducing bacteria. Terra Nova, 26(1): 72–77CrossRefGoogle Scholar
  5. Bosak T, Newman D K (2003). Microbial nucleation of calcium carbonate in the Precambrian. Geology, 31(7): 577–580CrossRefGoogle Scholar
  6. Braissant O, Decho A W, Dupraz C, Glunk C, Przekop K M, Visscher P T (2007). Exopolymeric substances of sulfate-reducing bacteria: interactions with calcium at alkaline pH and implication for formation of carbonate minerals. Geobiology, 5(4): 401–411CrossRefGoogle Scholar
  7. Camoin G F, Gautret P, Montaggioni L F, Cabioch G (1999). Nature and environmental significance of microbialites in Quaternary reefs: the Tahiti paradox. Sediment Geol, 126(1‒4): 271–304CrossRefGoogle Scholar
  8. Chave K, Deffeyes K, Weyl P, Garrels R, Thompson M (1962). Observations on the solubility of skeletal carbonates in aqueous solutions. Science, 137(3523): 33–34CrossRefGoogle Scholar
  9. Clapham D E (2007). Calcium Signaling. Cell, 131(6): 1047–1058CrossRefGoogle Scholar
  10. De Philippis R, Vincenzini M (1998). Exocellular polysaccharides from cyanobacteria and their possible applications. FEMS Microbiol Rev, 22(3): 151–175CrossRefGoogle Scholar
  11. Dickson J A D (2002). Fossil echinoderms as monitor of the Mg/Ca ratio of phanerozoic oceans. Science, 298(5596): 1222–1224CrossRefGoogle Scholar
  12. Folk R L, Land L S (1975). Mg/Ca ratio and salinity: two controls over crystallization of dolomite. AAPG Bull, 59(1): 60–68Google Scholar
  13. Goto N, Kawamura T, Mitamura O, Terai H (1999). Importance of extracellular organic carbon production in the total primary production by tidal-flat diatoms in comparison to phytoplankton. Mar Ecol Prog Ser, 190: 289–295CrossRefGoogle Scholar
  14. Groisman E A, Hollands K, Kriner M A, Lee E J, Park S Y, Pontes M H (2013). Bacterial Mg2+ homeostasis, transport, and virulence. Annu Rev Genet, 47(1): 625–646CrossRefGoogle Scholar
  15. Keith R R, Hogg S D (1995). Competitive binding of calcium and magnesium to streptococcal lipoteichoic acid. BBA-Gen Subjects, 1245(1): 94–98CrossRefGoogle Scholar
  16. Kenward P A, Fowle D A, Goldstein R H, Ueshima M, González L A, Roberts J A (2013). Ordered low-temperature dolomite mediated by carboxyl-group density of microbial cell walls. AAPG Bull, 97(11): 2113–2125CrossRefGoogle Scholar
  17. Krause S, Liebetrau V, Gorb S, Sanchez-Roman M, McKenzie J A, Treude T (2012). Microbial nucleation of Mg-rich dolomite in exopolymeric substances under anoxic modern seawater salinity: new insight into an old enigma. Geology, 40(7): 587–590CrossRefGoogle Scholar
  18. Lambert P A, Hancock I C, Baddiley J (1975a). Influence of alanyl ester residues on the binding of magnesium ions to teichoic acids. Biochem J, 151(3): 671–676CrossRefGoogle Scholar
  19. Lambert P A, Hancock I C, Baddiley J (1975b). The interaction of magnesium ions with teichoic acid. Biochem J, 149(3): 519–524CrossRefGoogle Scholar
  20. Land L S (1998). Failure to precipitate dolomite at 25°C from dilute solution despite 1000-fold oversaturation after 32 years. Aquat Geochem, 4(3): 361–368CrossRefGoogle Scholar
  21. Liu D, Dong H, Bishop ME, Zhang J, Wang H, Xie S, Wang S, Huang L, Eberl D D (2012). Microbial reduction of structural iron in interstratified illite-smectite minerals by a sulfate-reducing bacterium. Geobiology, 10(2): 150–162CrossRefGoogle Scholar
  22. McKenzie J A, Vasconcelos C (2009). Dolomite Mountains and the origin of the dolomite rock of which they mainly consist: historical developments and new perspectives. Sedimentology, 56(1): 205–219CrossRefGoogle Scholar
  23. Michiels J, Xi C, Verhaert J, Vanderleyden J (2002). The functions of Ca2+ in bacteria: a role for EF-hand proteins? Trends Microbiol, 10(2): 87–93CrossRefGoogle Scholar
  24. Moreno J, Vargas M, Olivares H, Rivas J N, Guerrero M G (1998). Exopolysaccharide production by the cyanobacterium Anabaena sp. ATCC 33047 in batch and continuous culture. J Biotechnol, 60(3): 175–182CrossRefGoogle Scholar
  25. Mucci A, Morse J W (1983). The incorporation of Mg2+ and Sr2+ into calcite overgrowths: influences of growth rate and solution composition. Geochim Cosmochim Acta, 47(2): 217–233CrossRefGoogle Scholar
  26. Qiu X, Wang H M, Liu D, Gong L F, Wu X P, Xiang X (2012). The physiological response of Synechococcus elongatus to salinity: a potential biomarker for ancient salinity in evaporative environments. Geomicrobiol J, 29(5): 477–483CrossRefGoogle Scholar
  27. Reeder R J, Sheppard C E (1984). Variation of lattice parameters in some sedimentary dolomites. Am Mineral, 69(5–6): 520–527Google Scholar
  28. Ries J B, Anderson M A, Hill R T (2008). Seawater Mg/Ca controls polymorph mineralogy of microbial CaCO3: a potential proxy for calcite-aragonite seas in Precambrian time. Geobiology, 6(2): 106–119CrossRefGoogle Scholar
  29. Sakaguchi T, Nakajima A (1982). Recovery of uranium by chitin phosphate and chitosan phosphate. Proceedings of the 2nd International Conference on Chitin and Chitosan, 177–182Google Scholar
  30. Sandberg P A (1983). An oscillating trend in Phanerozoic non-skeletal carbonate mineralogy. Nature, 305(5929): 19–22CrossRefGoogle Scholar
  31. Saunders P, Rogerson M, Wadhawan J D, Greenway G, Pedley H M (2014). Mg/Ca ratios in freshwater microbial carbonates: thermodynamic, kinetic and vital effects. Geochim Cosmochim Acta, 147: 107–118CrossRefGoogle Scholar
  32. Spadafora A, Perri E, McKenzie J A, Vasconcelos C (2010). Microbial biomineralization processes forming modern Ca:Mg carbonate stromatolites. Sedimentology, 57(1): 27–40CrossRefGoogle Scholar
  33. Stoupin D, Kiss A K, Arndt H, Shatilovich A V, Gilichinsky D A, Nitsche F (2012). Cryptic diversity within the choanoflagellate morphospecies complex Codosiga botrytis–Phylogeny and morphology of ancient and modern isolates. Eur J Protistol, 48(4): 263–273CrossRefGoogle Scholar
  34. Turner B F, Fein J B (2006). Protofit: a program for determining surface protonation constants from titration data. Comput Geosci, 32(9): 1344–1356CrossRefGoogle Scholar
  35. Van Lith Y, Warthmann R, Vasconcelos C, McKenzie J A (2003). Microbial fossilization in carbonate sediments: a result of the bacterial surface involvement in dolomite precipitation. Sedimentology, 50(2): 237–245CrossRefGoogle Scholar
  36. Wang D B, Wallace A F, De Yoreo J J, Dove P M (2009). Carboxylated molecules regulate magnesium content of amorphous calcium carbonates during calcification. Proc Natl Acad Sci USA, 106(51): 21511–21516CrossRefGoogle Scholar
  37. Wilson W W, Wade M M, Holman S C, Champlin F R (2001). Status of methods for assessing bacterial cell surface charge properties based on zeta potential measurements. J Microbiol Methods, 43(3): 153–164CrossRefGoogle Scholar
  38. Xu J, Yan C, Zhang F F, Konishi H, Xu H F, Teng H H (2013). Testing the cation-hydration effect on the crystallization of Ca–Mg–CO3 systems. Proc Natl Acad Sci USA, 110(44): 17750–17755CrossRefGoogle Scholar

Copyright information

© Higher Education Press and Springer-Verlag Berlin Heidelberg 2018

Authors and Affiliations

  • Xuan Qiu
    • 1
    • 2
  • Yanchen Yao
    • 2
  • Hongmei Wang
    • 1
    • 2
  • Yong Duan
    • 2
  1. 1.State Key Laboratory of Biogeology and Environmental GeologyChina University of GeosciencesWuhanChina
  2. 2.School of Environmental StudiesChina University of GeosciencesWuhanChina

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