Abstract
This study investigated the effect of environmental physical factors on the relative abundance of bacteria and the consequential landscape evolution in karst topography, focusing mainly on the effects of ureolytic microbial CaCO3 precipitation. The narrow-sky located in the upper part of Tangshan is a small gulch of Pleistocene coralline limestone formation in southern Taiwan. A 16S-metagenomic approach was used to determine the relationship of microbial community structures on the landscapes in various habitats. Our results showed that the biomass of habitats in the opening of the gulch was two times higher than the inside where light penetration was lower. We also found that speleothems only occurred at the inner wall inside the gulch, where the environment exhibited water drips running through the surface of speleothems and less light penetration. The sequence reads of operational taxonomic units relative to urease-producing bacteria and weathering-associated bacteria from each habitat were determined by NCBI database. Our data revealed that the 16S-metagenomics of the inner wall and water samples exhibited more sequences that were similar to those of urease-producing bacteria, whereas the outer wall showed more sequences that were similar to those of weathering-associated bacteria, suggesting that bacteria facilitated the formation of limestone weathering and calcite precipitation for various habitats. The semi-quantitative PCR for determining bacterial urease gene (ureC) levels confirmed that the inner limestone habitat had higher ureC gene levels than the outer limestone habitat. This study revealed the pivotal role of microorganisms in governing the geological evolution in the lightless limestone landscape.
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References
Abo-El-Enein SA, Ali AH, Talkhan FN, Abdel-Gawwad HA (2012) Utilization of microbial induced calcite precipitation for sand consolidation and mortar crack remediation. HBRC J 8:185–192. https://doi.org/10.1016/j.hbrcj.2013.02.001
Ahmed E, Holmström SJM (2015) Microbe–mineral interactions: the impact of surface attachment on mineral weathering and element selectivity by microorganisms. Chem Geol 403:13–23. https://doi.org/10.1016/j.chemgeo.2015.03.009
Anbu P, Kang C-H, Shin Y-J, So J-S (2016) Formations of calcium carbonate minerals by bacteria and its multiple applications. Springerplus. https://doi.org/10.1186/s40064-016-1869-2
Animesh S, Ramkrishnan R (2016) Study on effect of microbial induced calcite precipitates on strength of fine grained soils. Perspect Sci 8:198–202. https://doi.org/10.1016/j.pisc.2016.03.017
Barton HA, Northup DE (2007) Geomicrobiology in cave environments: past, current and future perspectives. J Cave Karst Stud 69(1):163–178
Barton LL, Mandl M, Loy A (2010) Geomicrobiology: molecular and environmental perspective. https://doi.org/10.1007/978-90-481-9204-5
Castanier S, Me ́tayer-Levrel GL, Perthuisot JP (1999) Ca-carbonates precipitation and limestone genesis—the microbiogeologist point of view. Sediment Geol 126:9–23
Ercole C, Cacchio P, Cappuccio G, Lepidi A (2001) Deposition of calcium carbonate in karst caves: role of bacteria in Stiffe’s cave. Int J Speleol 30A:69–79
Gat D, Tsesarsky M, Shamir D, Ronen Z (2014) Accelerated microbial-induced CaCO3 precipitation in a defined coculture of ureolytic and non-ureolytic bacteria. Biogeosciences 11:2561–2569
Hammes F, Boon N, Villiers J, Verstraete W, Siciliano S (2003) Strain-specific ureolytic microbial calcium carbonate precipitation. Appl Environ Microbiol 69:4901–4909. https://doi.org/10.1128/AEM.69.8.4901-4909.2003
Hsieh ML, Knuepfer PLK (2001) Middle–late Holocene river terraces in the Erhjen River Basin, southwestern Taiwan—implications of river response to climate change and active tectonic uplift. Geomorphology 38:337–372
Huang TY, Hsu BM, Chao WC, Fan CW (2018) Plant n-alkane production from litterfall altered the diversity and community structure of alkane degrading bacteria in litter layer in lowland subtropical rainforest in Taiwan. Biogeosciences 15:1815–1826. https://doi.org/10.5194/bg-15-1815-2018
Hutchens E (2009) Microbial selectivity on mineral surfaces: possible implications for weathering processes. Fungal Biol Rev 23:115–121. https://doi.org/10.1016/j.fbr.2009.10.002
Jacobson AD, Wu L (2009) Microbial dissolution of calcite at T = 28 °C and ambient pCO2. Geochim Cosmochim Acta 73:2314–2331. https://doi.org/10.1016/j.gca.2009.01.020
Jones B (2017) Review of calcium carbonate polymorph precipitation in spring systems. Sed Geol 353:64–75. https://doi.org/10.1016/j.sedgeo.2017.03.006
Kawano M, Obokata S (2007) Effects of cyanobacteria on precipitation rate and polymorphism of CaCO3 minerals in hot spring water. Nendo Kagaku 46:156–168
Kaźmierczak J, Coleman ML, Gruszczyński M, Kempe S (1996) Cyanobacterial key to the genesis of micritic and peloidal limestones in ancient seas. Acta Palaeontol Pol 41:319–338
Kumari D, Qian XY, Pan X, Achal V, Li Q, Gadd GM (2016) Microbially-induced carbonate precipitation for immobilization of toxic metals. Adv Appl Microbiol 94:79–108. https://doi.org/10.1016/bs.aambs.2015.12.002
Lacombe O, Angelier J, Chen HW, Deffontaines B, Chu HT, Rocher M (1997) Syndepositional tectonics and extension-compression relationships at the front of the Taiwan collision belt: a case study in the Pleistocene reefal limestones near Kaohsiung, SW Taiwan. Tectonophysics 274:83–96. https://doi.org/10.1016/S0040-1951(96)00299-5
Lian B, Chen Y, Zhu L, Yang R (2008) Effect of microbial weathering on carbonate rocks. Earth Sci Front 15:90–99
Lian B, Yuan D, Liu Z (2011) Effect of microbes on karstification in karst ecosystems. Chin Sci Bull 56:3743–3747. https://doi.org/10.1007/s11434-011-4648-z
Lower SK, Hochella MFJ, Beveridge TJ (2001) Bacterial recognition of mineral surfaces: nanoscale interactions between Shewanella and α-FeOOH. Science 292:1360–1363
Mitchell JK, Santamarina JC (2005) Biological considerations in geotechnical engineering. J Geotech Geoenviron Eng 131:1222–1233. https://doi.org/10.1061/(ASCE)1090-0241(2005)131:10(1222)
Mortensen BM, Haber MJ, DeJong JT, Caslake LF, Nelson DC (2011) Effects of environmental factors on microbial induced calcium carbonate precipitation. J Appl Microbiol 111:338–349. https://doi.org/10.1111/j.1365-2672.2011.05065.x
Omoregie AI (2016) Characterization of ureolytic bacteria isolated from limestone caves of sarawak and evaluation of their efficiency in biocementation. Swinburne University of Technology (Sarawak Campus), Malaysia. https://doi.org/10.13140/RG.2.2.11719.55205
Ortiz M, Neilson JW, Nelson WM, Legatzki A, Byrne A, Yu Y, Wing RA, Soderlund CA, Pryor BM, Pierson LS 3rd, Maier RM (2013) Profiling bacterial diversity and taxonomic composition on speleothem surfaces in Kartchner Caverns, AZ. Microb Ecol 65:371–383. https://doi.org/10.1007/s00248-012-0143-6
Ortiz M, Legatzki A, Neilson JW, Fryslie B, Nelson WM, Wing RA, Soderlund CA, Pryor BM, Maier RM (2014) Making a living while starving in the dark: metagenomic insights into the energy dynamics of a carbonate cave. ISME J 8:478–491. https://doi.org/10.1038/ismej.2013.159
Qabany A, Soga K, Santamarina C (2012) Factors affecting efficiency of microbially induced calcite precipitation. J Geotech Geoenviron Eng 138:992–1001. https://doi.org/10.1061/(ASCE)GT.1943-5606.0000666
Reed K (2008) Restriction enzyme mapping of bacterial urease genes: using degenerate primers to expand experimental outcomes. Biochem Mol Biol Educ 29:239–244. https://doi.org/10.1111/j.1539-3429.2001.tb00131.x
Seiffert F, Bandow N, Bouchez J, von Blanckenburg F, Gorbushina AA (2014) Microbial colonization of bare rocks: laboratory biofilm enhances mineral weathering. Procedia Earth Planet Sci 10:123–129. https://doi.org/10.1016/j.proeps.2014.08.042
Sulu-Gambari F (2011) Bacterially-induced dissolution of calcite: The role of bacteria in limestone weathering. McGill University Libraries, Montreal, QC
Tomczyk-Żak K, Zielenkiewicz U (2015) Microbial diversity in caves. Geomicrobiol J 33:20–38. https://doi.org/10.1080/01490451.2014.1003341
Uroz S, Calvaruso C, Turpault MP, Pierrat JC, Mustin C, Frey-Klett P (2007) Effect of the mycorrhizosphere on the genotypic and metabolic diversity of the bacterial communities involved in mineral weathering in a forest soil. Appl Environ Microbiol 73:3019–3027. https://doi.org/10.1128/AEM.00121-07
Uroz S, Calvaruso C, Turpault MP, Frey-Klett P (2009) Mineral weathering by bacteria: ecology, actors and mechanisms. Trends Microbiol 17:378–387. https://doi.org/10.1016/j.tim.2009.05.004
Wei S, Cui H, Jiang Z, Liu H, He H, Fang N (2015) Biomineralization processes of calcite induced by bacteria isolated from marine sediments. Braz J Microbiol 46:455–464. https://doi.org/10.1590/S1517-838246220140533
Wu Y-w, Zhang J-c, Wang L-j, Wang Y-x (2017) A rock-weathering bacterium isolated from rock surface and its role in ecological restoration on exposed carbonate rocks. Ecol Eng 101:162–169. https://doi.org/10.1016/j.ecoleng.2017.01.023
Xu G, Li D, Binquan J, Li D, Yin Y, Lun L, Zhao Z, Li S (2016) Biomineralization of a calcifying ureolytic bacterium Microbacterium sp. GM-1. Electron J Biotechnol. https://doi.org/10.1016/j.ejbt.2016.10.008
Yun Y, Wang H, Man B, Xiang X, Zhou J, Qiu X, Duan Y, Engel AS (2016) The Relationship between pH and bacterial communities in a single karst ecosystem and its implication for soil acidification. Front Microbiol. https://doi.org/10.3389/fmicb.2016.01955
Zepeda Mendoza ML, Lundberg J, Ivarsson M, Campos P, Nylander JA, Sallstedt T, Dalen L (2016) Metagenomic analysis from the interior of a speleothem in Tjuv-Ante’s Cave, Northern Sweden. PLoS ONE 11:e0151577. https://doi.org/10.1371/journal.pone.0151577
Zhou JP, Huang Y, Mo MH (2009) Phylogenetic analysis on the soil bacteria distributed in karst forest. Braz J Microbiol 40:827–837
Zhu T, Dittrich M (2016) Carbonate precipitation through microbial activities in natural environment, and their potential in biotechnology: a review. Front Bioeng Biotechnol. https://doi.org/10.3389/fbioe.2016.00004
Acknowledgements
This research was supported by the Ministry of Science and Technology of Taiwan (MOST 109-2116-M-194-013 and 109-2116-M-194-012). This research was also supported by Ditmanson Medical Foundation Chia-Yi Christian Hospital (RCN007) and the Center for Innovative Research on Aging Society (CIRAS) from The Featured Areas Research Center Program within the framework of the Higher Education Sprout Project by the Ministry of Education (MOE) in Taiwan.
Funding
This study was funded by Ministry of Science and Technology, Taiwan (MOST 108-2811-M-194 -507 -, MOST 108-2116-M-194 -005 -), Buddhist Tzu Chi Medical Foundation (TCRD 108-39) and Ditmanson Medical Foundation Chia‐Yi Christian Hospital‐National Chung Cheng University Joint Research Program, CYCH‐CCU Joint Research Program (CYCH‐CCU‐2021).
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Conceptualization, F.-C.Y, B.-M.H, J.-S.C and C.-W.F; Methodology, T.-Y.H, H.-C.T and J.-S.C; Software, H.-C.T and J.-S.C; Validation, C.-W.F, J.-S.C and S.-W.H; Formal Analysis, B.-M.H, J.-S.C and C.-W.F; Investigation, J.-S.C, S.-W.H, H.-C.T and C.-Y.T; Resources, C.-W.F; Data Curation, J.-S.C, H.-C.T and T.-Y.H; Writing-Original Draft Preparation, J.-S.C, F.-C.Y and C.-W.F; Writing-Review and Editing, J.-S.C, B.-M.H, T.-Y.H, V.N and C.-W.F; Visualization, B.-M.H and F.-C.Y; Supervision, S.-W.H, B.-M.H, T.-Y.H, V.N and J.-S.C; Project Administration, J.-S.C, B.-M.H, T.-Y.H and C.-W.F; Funding Acquisition, B.-M.H, F.-C.Y and C.-W.F.
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Chen, JS., Tsai, HC., Hsu, BM. et al. The role of bacterial community in the formation of a stalactite in coral limestone areas of Taiwan by 16S rRNA gene amplicon surveys. Environ Earth Sci 80, 665 (2021). https://doi.org/10.1007/s12665-021-09969-w
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DOI: https://doi.org/10.1007/s12665-021-09969-w