Abstract
Bacterially induced precipitation of minerals leading to cementation of natural geological formations has been well recorded in a variety of environments. A range of microbial pathways and geochemical processes have been found to influence the cementation processes; but detailed formation mechanisms and biogeochemical relationships are still not very clear. There has been a growing demand for the application of bacterially driven biocementation in a number of geotechnical engineering applications recently. Here, we aimed to unpin the mechanisms behind the formation of actively mineralising beachrock sediments at Lucky Bay in Western Australia to understand the natural accretionary processes and potential of indigenous bacterial communities in biocementation. We observed ferruginous, aluminosilicate and carbonate cements along with extensive extra polymeric substances, borings with possible microbial activities in certain sections of native beachrock sediments. Cement precipitation under calcium- and iron-rich microenvironments sourced from seawater and iron creek seems to be driven by both biogenic and abiogenic processes in nature. Native microbial communities with a dominance of the genera Halococcus and Marinobacter were recorded. Enrichment of native bacterial communities under seawater media conditions was conducted which lead to successful biomineralisation of calcitic and ferruginous cements under in vitro conditions although the community composition changed significantly. Nanomechanical properties of natural and laboratory synthesised cement crystals showed that engineered biocement is highly promising. The results of this study clearly demonstrate biological influence in the formation of natural cements and hint significant potential of biostimulation which can be harnessed for different engineering applications including coastal erosion.
This is a preview of subscription content, access via your institution.










References
Adetutu E, Thorpe K, Shahsavari E, Bourne S, Cao X, Fard R, Kirby G, Ball A (2012) Bacterial community survey of sediments at Naracoorte caves, Australia. Int J Speleol 41(2):137–147. https://doi.org/10.5038/1827-806x.41.2.2
Albright R, Langdon C, Anthony KRN (2013) Dynamics of seawater carbonate chemistry, production, and calcification of a coral reef flat, central great barrier reef. Biogeosciences 10:6747–6758
Alexandersson T (1969) Recent littoral and sublittoral high-mg calcite lithification in the mediterranean. Sedimentology 12:47–61
Anbu P, Kang CH, Shin YJ, So JS (2016) Formations of calcium carbonate minerals by bacteria and its multiple applications. Springerplus 5:250. https://doi.org/10.1186/s40064-016-1869-2
Aramendia J, Gomez-Nubla L, Arrizabalaga I, Prieto-Taboada N, Castro K, Madariaga JM (2013) Multianalytical approach to study the dissolution process of weathering steel: the role of urban pollution. Corros Sci 76:154–162. https://doi.org/10.1016/j.corsci.2013.06.038
Arrieta N, Iturregui A, Martinez-Arkarazo I, Murelaga X, Baceta JI, de Diego A, Olazabal MA, Madariaga JM (2017) Characterization of ferruginous cements related with weathering of slag in a temperate anthropogenic beachrock. Sci Total Environ 581-582:49–65. https://doi.org/10.1016/j.scitotenv.2016.12.132
Banerjee S, Joshi SR (2014) Ultrastructural analysis of calcite crystal patterns formed by biofilm bacteria associated with cave speleothems. J Microsc Ultrastruct 2(4):217–223. https://doi.org/10.1016/j.jmau.2014.06.001
Berges JA, Franklin DJ, Harrison PJ (2001) Evolution of an artificial sea water medium: improvements in enriched seawater, artificial water over the last two decades. J Phycol 37(6):1138–1145. https://doi.org/10.1046/j.1529-8817.2001.01052.x
Calvaresi M, Falini G, Pasquini L, Reggi M, Fermani S, Gazzadi GC, Frabboni S, Zerbetto F (2013) Morphological and mechanical characterization of composite calcite/SWCNT-COOH single crystals. Nanoscale 5(15):6944–6949
Castro-Alonso MJ, Montañez-Hernandez LE, Sanchez-Muñoz MA, Macias Franco MR, Narayanasamy R, Balagurusamy N (2019) Microbially induced calcium carbonate precipitation (MICP) and its potential in bioconcrete: microbiological and molecular concepts. Front Mater 6(126). https://doi.org/10.3389/fmats.2019.00126
Chan CS, De Stasio G, Welch SA, Girasole M, Frazer BH, Nesterova MV, Fakra S, Banfield JF (2004) Microbial polysaccharides template assembly of nanocrystal fibers. Science 303(5664):1656–1658. https://doi.org/10.1126/science.1092098
Chan CS, Fakra SC, Emerson D, Fleming EJ, Edwards KJ (2010) Lithotrophic iron-oxidizing bacteria produce organic stalks to control mineral growth: implications for biosignature formation. Isme J 5:717. https://doi.org/10.1038/ismej.2010.173 https://www.nature.com/articles/ismej2010173#supplementary-information
Chandrasekaran A, Rajalakshmi A, Ravisankar R, Kalarasai S (2015) Analysis of beach rock samples of Andaman Island, India by spectroscopic techniques. J Basic Appl Zool 2(1):55–64. https://doi.org/10.1016/j.ejbas.2014.12.004
Chicot D, Mendoza J, Zaoui A, Louis G, Lepingle V, Roudet F, Lesage J (2011) Mechanical properties of magnetite (Fe3O4), hematite (α-Fe2O3) and goethite (α-FeO·OH) by instrumented indentation and molecular dynamics analysis. Mater Chem Phys 129(3):862–870. https://doi.org/10.1016/j.matchemphys.2011.05.056
Chivas A, Chappell J, Polach H, Pillans B, Flood P (1986) Radiocarbon evidence for the timing and rate of island development, beach rock formation and phosphatization at Lady Elliot island, Queensland, Australia. Mar Geol 69:273–287
Cook DC (2005) Spectroscopic identification of protective and non-protective corrosion coatings on steel structures in marine environments. Corros Sci 47:2550–2570
de Faria DLA, Lopes FN (2007) Heated goethite and natural hematite: can Raman spectroscopy be used to differentiate them? Vib Spectrosc 45(2):117–121. https://doi.org/10.1016/j.vibspec.2007.07.003
DeJong JT, Kavazanjian E (2019) Bio-mediated and bio-inspired geotechnics. In: Lu N, Mitchell JK (eds) Geotechnical fundamentals for addressing New World Challenges, Series in Geomechanics and Geoengineering. Springer, Berlin, pp 193–207
Dejong JT, Soga K, Kavazanjian E, Burns S, Van Paassen LA, Al Qabany A, Aydilek A, Bang SS, Burbank M, Caslake LF, Chen CY, Cheng X, Chu J, Ciurli S, Esnault-Filet A, Fauriel S, Hamdan N, Hata T, Inagaki Y, Jefferis S, Kuo M, Laloui L, Larrahondo J, Manning DAC, Martinez B, Montoya BM, Nelson DC, Palomino A, Renforth P, Santamarina JC, Seagren EA, Tanyu B, Tsesarsky M, Weaver T (2013) Biogeochemical processes and geotechnical applications: progress, opportunities and challenges. Géotechnique 63(4):287–301. https://doi.org/10.1680/geot.SIP13.P.017
Dhami NK, Reddy MS, Mukherjee A (2013a) Biomineralization of calcium carbonate polymorphs by the bacterial strains isolated from calcareous sites. J Microbiol Biotechnol 23(5):707–714. https://doi.org/10.4014/jmb.1212.11087
Dhami NK, Reddy MS, Mukherjee A (2013b) Biomineralization of calcium carbonates and their engineered applications: a review. Front Microbiol 4:314. https://doi.org/10.3389/fmicb.2013.00314
Dhami NK, Mukherjee A, Reddy MS (2016) Micrographical, minerological and nano-mechanical characterisation of microbial carbonates from urease and carbonic anhydrase producing bacteria. Ecol Eng 94:443–454. https://doi.org/10.1016/j.ecoleng.2016.06.013
Dhami NK, Alsubhi WR, Watkin E, Mukherjee A (2017) Bacterial community dynamics and biocement formation during stimulation and augmentation: implications for soil consolidation. Front Microbiol 8:1267. https://doi.org/10.3389/fmicb.2017.01267
Dhami NK, Mukherjee A, Watkin ELJ (2018) Microbial diversity and mineralogical-mechanical properties of calcitic cave speleothems in natural and in vitro biomineralization conditions. Front Microbiol 9:40. https://doi.org/10.3389/fmicb.2018.00040
Dickinson WR (1999) Holocene Sea level record on Funafuti and potential impact of global warming on Central Pacific atolls. Quat Res 51(2):181–189
Easton WH (1974) An unusual inclusion in beach rock. J Sediment Petrol 44:693–694
Emerson D, Fleming EJ, McBeth JM (2010) Iron-oxidizing bacteria: an environmental and genomic perspective. Annu Rev Microbiol 64:561–583
Ercole EC, Bozzelli P, Altieri F, Cacchio P, Del Gallo M (2012) Calcium carbonate mineralization: involvement of extracellular polymeric materials isolated from calcifying bacteria. Microsc Microanal 18:829–839
Fortin D, Langley S (2005) Formation and occurrence of biogenic iron-rich minerals. Earth Sci Rev 72(1):1–19. https://doi.org/10.1016/j.earscirev.2005.03.002
García GM, Márquez GMA, Moreno HCX (2016) Characterization of bacterial diversity associated with calcareous deposits and drip-waters, and isolation of calcifying bacteria from two Colombian mines. Microbiol Res 182:21–30. https://doi.org/10.1016/j.micres.2015.09.006
Glaring MA, Vester JK, Lylloff JE, Abu Al-Soud W, Sørensen SJ, Stougaard P (2015) Microbial diversity in a permanently cold and alkaline environment in Greenland. PLoS One 10(4):e0124863. https://doi.org/10.1371/journal.pone.0124863
Hamdan N, Kavazanjian E, Rittmann BE, Karatas I (2016) Carbonate mineral precipitation for soil improvement through microbial denitrification. Geomicrobiol J 34(2):139–146. https://doi.org/10.1080/01490451.2016.1154117
Hedrich S, Schlömann M, Johnson DB (2011) The iron-oxidizing proteobacteria. Microbiology 157(6):1551–1564. https://doi.org/10.1099/mic.0.045344-0
Honeyands T, Manuel J, Matthews L, O’Dea D, Pinson D, Leedham J, Zhang G, Li H, Monaghan B, Liu X, Donskoi E, Webster NAS, Pownceby MI (2019) Comparison of the mineralogy of iron ore sinters using a range of techniques. Minerals 9(333):1–17. https://doi.org/10.3390/min9060333
Iturregui A, Arrieta N, Murelaga X, Baceta JI, Olazabal MA, Martínez-Arkarazoa I, Madariagaa JM (2014) The relevance of the analytical methodology in the geochemical study of beachrock outcrops: Arrigunaga Beach inside the Nerbioi-Ibaizabal estuary (Getxo, Basque Country). Anal Methods 6:329–336
Jubb AM, Allen HC (2010) Vibrational spectroscopic characterization of hematite, maghemite, and magnetite thin films produced by vapor deposition. ACS Appl Mater Interfaces 2(10):2804–2812. https://doi.org/10.1021/am1004943
Kato S, Chan C, Itoh T, Ohkuma M (2013) Functional gene analysis of freshwater iron-rich flocs at circumneutral pH and isolation of a stalk-forming microaerophilic iron-oxidizing bacterium. Appl Environ Microbiol 79(17):5283–5290. https://doi.org/10.1128/AEM.03840-12
Khan M, Danjo T, Kawasaki S (2015) Artificial beach rock formation through sand solidification towards inhibition of coastal erosion in Bangladesh. Int J Geomater 9:1528–1533
Kooli WM, Comensoli L, Maillard J, Albini M, Gelb A, Junier P, Joseph E (2018) Bacterial iron reduction and biogenic mineral formation for the stabilisation of corroded iron objects. Sci Rep 8(1):764. https://doi.org/10.1038/s41598-017-19020-3
McCutcheon J, Nothdurft LD, Webb GE, Paterson D, Southam G (2016) Beachrock formation via microbial dissolution and re-precipitation of carbonate minerals. Mar Geol 382:122–135. https://doi.org/10.1016/j.margeo.2016.10.010
Meyers JH (1987) Marine vadose beach rock cementation by cryptocrystalline magnesian calcite – Maui. Hawaii J Sediment Petrol 57:558–570
Moore CH (1973) Intertidal carbonate cementation, grand Cayman, West Indies. J Sediment Petrol 43:591–602
Müller WEG, Neufurth M, Schlossmacher U, Schröder HC, Pisignano D, Wang X (2014) The sponge silicatein-interacting protein silintaphin-2 blocks calcite formation of calcareous sponge spicules at the vaterite stage. RSC Adv 4:2577–2585
Porter H, Dhami NK, Mukherjee A (2017) Synergistic chemical and microbial cementation for stabilization of aggregates. Cem Concr Compos 83:160–170. https://doi.org/10.1016/j.cemconcomp.2017.07.015
Porter H, Dhami NK, Mukherjee A (2018) Sustainable road bases with microbial precipitation. Proc Inst Civ Eng Constr Mater 171(3):95–108. https://doi.org/10.1680/jcoma.16.00075
Presser V, Gerlach K, Vohrer A, Nickel KG, Dreher WF (2010) Determination of the elastic modulus of highly porous samples by nanoindentation: a case study on sea urchin spines. J Mater Sci 45(9):2408–2418. https://doi.org/10.1007/s10853-010-4208-y
Raybaud V, Tambutté S, Ferrier-Pagès C, Reynaud S, Venn AA, Tambutté É, Nival P, Allemand D (2017) Computing the carbonate chemistry of the coral calcifying medium and its response to ocean acidification. J Theor Biol 424:26–36. https://doi.org/10.1016/j.jtbi.2017.04.028
Ren D, Meyers MA, Zhou B, Feng Q (2013) Comparative study of carp otolith hardness: lapillus and asteriscus. Mater Sci Eng C Mater Biol Appl 33(4):1876–1881. https://doi.org/10.1016/j.msec.2012.10.015
Rodriguez-Navarro C, Jroundi F, Schiro M, Ruiz-Agudo E, Gonzalez-Munoz MT (2012) Influence of substrate mineralogy on bacterial mineralization of calcium carbonate: implications for stone conservation. Appl Environ Microbiol 78(11):4017–4029. https://doi.org/10.1128/AEM.07044-11
Rusell RJ, McIntire WG (1965) Southern hemisphere beach rock. Geogr Rev 55:17–45
Rusznyak A, Akob DM, Nietzsche S, Eusterhues K, Totsche KU, Neu TR, Frosch T, Popp J, Keiner R, Geletneky J, Katzschmann L, Schulze ED, Küsel K (2012) Calcite biomineralization by bacterial isolates from the recently discovered pristine karstic Herrenberg cave. Appl Environ Microbiol 78(4):1157–1167. https://doi.org/10.1128/AEM.06568-11
Sanchez-Roman M, Puente-Sanchez F, Parro V, Amils R (2015) Nucleation of Fe-rich phosphates and carbonates on microbial cells and exopolymeric substances. Front Microbiol 6:1024. https://doi.org/10.3389/fmicb.2015.01024
Scoffin TP, Stoddart DR (1983) Beachrock and intertidal cements. In: Goudie AS, Pye K (eds) Chemical sediments and geomorphology. Academic Press, London, pp 401–425
Shen J-W, Long J-P, Pedoja K, Yang H-Q, Xu H-L, Sun J-L (2013) Holocene coquina beachrock from Haishan Island, east coast of Guangdong Province, China. Quat Int 310:199–212. https://doi.org/10.1016/j.quaint.2013.05.011
Stocks-Fischer S, Galinat JK, Bang SS (1999) Microbiological precipitation of CaCO3. Soil Biol Biochem 31:1563–1571
Strasser A, Bernier P (1988) Early diagenetic ferruginous cementation in the intertidal zone: example from Noirmoutier Island, France. Oceanol Acta 11:353–357
Strobel R, Pratsinis SE (2009) Direct synthesis of maghemite, magnetite and wustite nanoparticles by flame spray pyrolysis. Adv Powder Technol 20(2):190–194. https://doi.org/10.1016/j.apt.2008.08.002
Takeshita Y, Cyronak T, Martz TR, Kindeberg T, Andersson AJ (2018) Coral reef carbonate chemistry variability at different functional scales. Front Mar Sci 5(175):1–12. https://doi.org/10.3389/fmars.2018.00175
Vousdoukas MI, Velegrakis AF, Plomaritis TA (2007) Beachrock occurrence, characteristics, formation mechanisms and impacts. Earth-Science Rev 85(1):23–46. https://doi.org/10.1016/j.earscirev.2007.07.002
Yoshida DH, Yamamoto K, Murakami Y, Matsuoka K (2006) Formation of biogenic iron-oxide nodules in reducing sediments as an analogue of near-field redox reaction products. Phys Chem Earth Parts A/B/C 31(10–14):593–599. https://doi.org/10.1016/j.pce.2006.04.009
Zamarreno DV, Inkpen R, May E (2009) Carbonate crystals precipitated by freshwater bacteria and their use as a limestone consolidant. Appl Environ Microbiol 75(18):5981–5990. https://doi.org/10.1128/AEM.02079-08
Zamiri A, De S (2011) Mechanical properties of hydroxyapatite single crystals from nanoindentation data. J Mech Behav Biomed 4(2):146–152. https://doi.org/10.1016/j.jmbbm.2010.11.001
Zeng Z, Tice MM (2014) Promotion and nucleation of carbonate precipitation during microbial iron reduction. Geobiology 12(4):362–371. https://doi.org/10.1111/gbi.12090
Zhu T, Dittrich M (2016) Carbonate precipitation through microbial activities in natural environment, and their potential in biotechnology: a review. Front Bioeng Biotechnol 4:4. https://doi.org/10.3389/fbioe.2016.00004
Zhu W, Hughes JJ, Bicanic N, Pearce CJ (2007) Nanoindentation mapping of mechanical properties of cement paste and natural rocks. Mater Charact 58(11–12):1189–1198. https://doi.org/10.1016/j.matchar.2007.05.018
Acknowledgements
The authors acknowledge the use of Curtin University’s Microscopy, Microanalysis and Chemical analysis Facility at John de Laeter Research Centre whose instrumentation has been partially funded by the University, State and Commonwealth Governments. The authors also thank TSW Analytical (Perth, Australia) for their help with ICP-MS testing. The authors thank Dr. Anna Heitz from the Department of Civil Engineering at Curtin University for her help with sampling and fieldwork. The authors thank Ms. Sakshi Tiwari from the Department of Civil Engineering at Curtin University for her help with bacterial sequencing analysis.
Funding
The funding for this study was provided by Curtin University, Western Australia, Australia.
Author information
Authors and Affiliations
Contributions
ND contributed to the concepts and ideas, fieldwork, designing of research, supervision of experiments, analysis of data and writing. AR contributed to the fieldwork, experiments, analysis of data. PP contributed to the experiments and analysis of data. AM contributed to the fieldwork and analysis of data. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
The article does not contain any studies with human participants or animals performed by any of the authors.
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(PDF 194 kb)
Rights and permissions
About this article
Cite this article
Ramachandran, A.L., Polat, P., Mukherjee, A. et al. Understanding and creating biocementing beachrocks via biostimulation of indigenous microbial communities. Appl Microbiol Biotechnol 104, 3655–3673 (2020). https://doi.org/10.1007/s00253-020-10474-6
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-020-10474-6
Keywords
- Beachrocks
- Biodiversity
- Biocement
- Calcium carbonate minerals
- Ferruginous minerals
- Nanomechanical characterisation