喀斯特洞穴细菌群落的生境特异性及其潜在功能：以广西桂林盘龙洞为例

曾智霖; 程晓钰; 王红梅; 曹静; 杨梓琪; 刘晓燕; 王昳衡; 李璐; 苏春田; 黄奇波

doi:10.3799/dqkx.2022.068

Volume 48 Issue 12

Dec. 2023

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Article Navigation > Earth Science > 2023 > 48(12): 4711-4726

Zeng Zhilin, Cheng Xiaoyu, Wang Hongmei, Cao Jing, Yang Ziqi, Liu Xiaoyan, Wang Yiheng, Li Lu, Su Chuntian, Huang Qibo, 2023. Niche Specificity and Potential Functions of Microbial Communities in Karst Caves as Exampled by Panlong Cave in Guilin City, Guangxi. Earth Science, 48(12): 4711-4726. doi: 10.3799/dqkx.2022.068

Citation:

Zeng Zhilin, Cheng Xiaoyu, Wang Hongmei, Cao Jing, Yang Ziqi, Liu Xiaoyan, Wang Yiheng, Li Lu, Su Chuntian, Huang Qibo, 2023. Niche Specificity and Potential Functions of Microbial Communities in Karst Caves as Exampled by Panlong Cave in Guilin City, Guangxi. Earth Science, 48(12): 4711-4726. doi: 10.3799/dqkx.2022.068

Citation:

Zeng Zhilin, Cheng Xiaoyu, Wang Hongmei, Cao Jing, Yang Ziqi, Liu Xiaoyan, Wang Yiheng, Li Lu, Su Chuntian, Huang Qibo, 2023. Niche Specificity and Potential Functions of Microbial Communities in Karst Caves as Exampled by Panlong Cave in Guilin City, Guangxi. Earth Science, 48(12): 4711-4726. doi: 10.3799/dqkx.2022.068

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Niche Specificity and Potential Functions of Microbial Communities in Karst Caves as Exampled by Panlong Cave in Guilin City, Guangxi

doi: 10.3799/dqkx.2022.068

Zeng Zhilin^{1, 2
,
,},
Cheng Xiaoyu^{1, 2},
Wang Hongmei^{1, 2
,
,
,},
Cao Jing^{1, 2},
Yang Ziqi^{1, 2},
Liu Xiaoyan^{1, 2},
Wang Yiheng^{1, 2},
Li Lu^{1, 2},
Su Chuntian³,
Huang Qibo³

1.
School of Environmental Studies, China University of Geosciences, Wuhan 430078, China
2.
State Key Laboratory of Geobiology and Environmental Geology, China University of Geosciences, Wuhan 430078, China
3.
Institute of Karst Geology, China Geological Survey, Guilin 541000, China

Received Date: 2021-12-24
Available Online: 2024-01-03
Publish Date: 2023-12-25

Abstract

Abstract

Karst caves serve as the natural laboratories to study subsurface biosphere, which provide ideal places to investigate microbial diversity and their interactions between microbes and environments. Guilin is one of the typical areas with developed karst landscape. Deep investigation of cave microbes in different niches and their response to environmental variables will provide valuable information on subsurface biosphere in terms of microbial diversity, function and interaction with environments. To this end, Samples were collected from overlying soils, sediments, cave wall, weathered crusted on cave walls, microbial biofilm on stalagmite surface and dripping water in the Panlong Cave in Guiling City to study microbial communities and their correlation with environmental variables via high throughput sequencing of 16S rRNA. Results show that bacterial communities show high specificity to niches and were dominated by Actinomycete and Proteobacteria. Each niche has its own specific indicator group. For example, Paemibacillus was the indicator for microbial biofilm on the dry surface of stalagmite, whilst Acidobacteriaceae and Pseudomonas were the indicator groups in microbial biofilm on the wet surface of stalagmite. Pseudomonadales and Branhamella were the indicator groups in dripping water, whereas indicator groups in overlying soils included Mycobacterium and Nocardioides. Bacillus and Gp-7 were indicators in sediments, whilst Chromatiales, Soilrubrobacteraceae and Rubrobcter were indicators in cave wall and Methylobacterium in weathered crust. Temperature was demonstrated to be the main variable impacting bacterial communities in the Panlong Cave as indicated by redundancy analysis. Tax4fun2 analysis shows that microbes participated in carbon and nitrogen cycles also varied with niches. Microbes in dripping water, microbial biofilm on dry/wet surface of stalagmite were closely related to nitrogen cycle. On the contrast, those in weathered crust, sediments and cave wall were more involved in carbon fixation. Co-occurrence network analysis inferred that corporation was the main strategy for microbial groups to survive in the oligotrophic karst caves.
- karst cave,
- subsurface biosphere,
- carbon fixation,
- nitrogen cycle,
- co-occurrence network,
- geomicrobiology

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References(67)

References

Barton, H. A., Giarrizzo, J. G., Suarez, P., et al., 2014. Microbial Diversity in a Venezuelan Orthoquartzite Cave is Dominated by the Chloroflexi (Class Ktedonobacterales) and Thaumarchaeota Group Ⅰ. 1c. Frontiers in Microbiology, 5: 615. https://doi.org/10.3389/fmicb.2014.00615

Bastida, F., Selevsek, N., Torres, I. F., et al., 2015. Soil Restoration with Organic Amendments: Linking Cellular Functionality and Ecosystem Processes. Scientific Reports, 5: 15550. https://doi.org/10.1038/srep15550

Bokulich, N. A., Thorngate, J. H., Richardson, P. M., et al., 2014. Microbial Biogeography of Wine Grapes is Conditioned by Cultivar, Vintage, and Climate. Proceedings of the National Academy of Sciences of the United States of America, 111(1): E139-E148. https://doi.org/10.1073/pnas.1317377110

Bradford, M. A., McCulley, R. L., Crowther, T. W., et al., 2019. Cross-Biome Patterns in Soil Microbial Respiration Predictable from Evolutionary Theory on Thermal Adaptation. Nature Ecology & Evolution, 3(2): 223-231. https://doi.org/10.1038/s31559-018-0771-4

Cai, Y. F., Zhou, X., Shi, L. M., et al., 2020. Atmospheric Methane Oxidizers are Dominated by Upland Soil Cluster Alpha in 20 Forest Soils of China. Microbial Ecology, 80(4): 859-871. https://doi.org/10.1007/s00248-020-01570-1

Caporaso, J. G., Kuczynski, J., Stombaugh, J., et al., 2010. QIIME Allows Analysis of High-Throughput Community Sequencing Data. Nature Methods, 7(5): 335-336. https://doi.org/10.1038/nmeth.f.303

Cheeptham, N., Sadoway, T., Rule, D., et al., 2013. Cure from the Cave: Volcanic Cave Actinomycetes and Their Potential in Drug Discovery. International Journal of Speleology, 42(1): 35-47. https://doi.org/10.5038/1827-806x.42.1.5

Cheng, S. B., Liu, A. S., Cui, S., et al., 2021. Mineralization Process of Permian Karst Bauxite in Western Guangxi. Earth Science, 46(8): 2697-2710(in Chinese with English abstract).

Cheng, X. Y., Liu, X. Y., Wang, H. M., et al., 2021a. USCγ Dominated Community Composition and Cooccurrence Network of Methanotrophs and Bacteria in Subterranean Karst Caves. Microbiology Spectrum, 9(1): e0082021. https://doi.org/10.1128/spectrum.00820-21

Cheng, X. Y., Yun, Y., Wang, H. M., et al., 2021b. Contrasting Bacterial Communities and Their Assembly Processes in Karst Soils under Different Land Use. Science of the Total Environment, 751: 142263. https://doi.org/10.1016/j.scitotenv.2020.142263

Claesson, M., O'Sullivan, Ó., Wang, Q., et al., 2009. Comparative Analysis of Pyrosequencing and a Phylogenetic Microarray for Exploring Microbial Community Structures in the Human Distal Intestine. PloS One, 4(8): e6669. https://doi.org/10.1371/journal.pone.0006669

Davis, M. C., Messina, M. A., Nicolosi, G., et al., 2020. Surface Runoff Alters Cave Microbial Community Structure and Function. PLoS One, 15(5): e0232742. https://doi.org/10.1371/journal.pone.0232742

Debora, R., Tugba, O., 2016. Carbon Dioxide Sequestration through Microbially-Induced Calcium Carbonate Precipitation Using Ureolytic Aquatic Microorganisms. Abstracts of Papers of the American Chemical Society, 251: 672-680.

Edgar, R. C., 2010. Search and Clustering Orders of Magnitude Faster than BLAST. Bioinformatics, 26(19): 2460-2461. https://doi.org/10.1093/bioinformatics/btq461

Edgar, R. C., Haas, B. J., Clemente, J. C., et al., 2011. UCHIME Improves Sensitivity and Speed of Chimera Detection. Bioinformatics, 27(16): 2194-2200. https://doi.org/10.1093/bioinformatics/btr381

Fang, B. Z., Salam, N., Han, M. X., et al., 2017. Insights on the Effects of Heat Pretreatment, pH, and Calcium Salts on Isolation of Rare Actinobacteria from Karstic Caves. Frontiers in Microbiology, 8: 1535. https://doi.org/10.3389/fmicb.2017.01535

Gulecal-Pektas, Y., 2016. Bacterial Diversity and Composition in Oylat Cave (Turkey) with Combined Sanger/Pyrosequencing Approach. Polish Journal of Microbiology, 65: 69-75. https://doi.org/10.5604/17331331.1197277

Han, Q., Ma, Q., Chen, Y., et al., 2020. Variation in Rhizosphere Microbial Communities and Its Association with the Symbiotic Efficiency of Rhizobia in Soybean. The ISME Journal, 14(8): 1915-1928. https://doi.org/10.1038/s31396-020-0648-9

He, Z. L., Gentry, T. J., Schadt, C. W., et al., 2007. GeoChip: A Comprehensive Microarray for Investigating Biogeochemical, Ecological and Environmental Processes. The ISME Journal, 1(1): 67-77. https://doi.org/10.1038/ismej.2007.2

Herbst, F. A., Jehmlich, N., von Bergen, M., et al., 2018. Sulfur-³⁴S and ³⁶S Stable Isotope Labeling of Amino Acids for Quantification (SULAQ34/36) of Proteome Analyses. Microbial Proteomics. Humana Press, New York, 163-174. https://doi.org/10.1007/978-1-4939-8695-8_12

Ivanova, A. A., Zhelezova, A. D., Chernov, T. I., et al., 2020. Linking Ecology and Systematics of Acidobacteria: Distinct Habitat Preferences of the Acidobacteriia and Blastocatellia in Tundra Soils. PLos One, 15(3): e0230157. https://doi.org/10.1371/journal.pone.0230157

Jones, D. S., Lyon, E., Macalady, J., 2008. Geomicrobiology of Biovermiculations from the Frasassi Cave System, Italy. Journal of Cave and Karst Studies, 70: 78-93.

Knief, C., 2015. Diversity and Habitat Preferences of Cultivated and Uncultivated Aerobic Methanotrophic Bacteria Evaluated Based on PMOA as Molecular Marker. Frontiers in Microbiology, 6: 1346. https://doi.org/10.3389/fmicb.2015.01346

Knief, C., Lipski, A., Dunfield, P. F., 2003. Diversity and Activity of Methanotrophic Bacteria in Different Upland Soils. Applied and Environmental Microbiology, 69(11): 6703-6714. https://doi.org/10.1128/aem.69.11.6703-6714.2003

Kontro, M., Lignell, U., Hirvonen, M. R., et al., 2005. pH Effects on 10 Streptomyces spp. Growth and Sporulation Depend on Nutrients. Letters in Applied Microbiology, 41(1): 32-38. https://doi.org/10.1111/j.1472-765x.2005.01727.x

Kraft, B., Tegetmeyer, H. E., Sharma, R., et al., 2014. The Environmental Controls That Govern the End Product of Bacterial Nitrate Respiration. Science, 345(6197): 676-679. https://doi.org/10.1126/science.1254070

Kranjc, A., 2011. The Origin and Evolution of the Term "Karst". Procedia—Social and Behavioral Sciences, 19: 567-570. https://doi.org/10.1016/j.sbspro.2011.05.170

Kuypers, M. M. M., Marchant, H. K., Kartal, B., et al., 2018. The Microbial Nitrogen-Cycling Network. Nature Reviews Microbiology, 16(5): 263-276. https://doi.org/10.1038/nrmicro.2018.9

Lavoie, K. H., Winter, A. S., Read, K. J. H., et al., 2017. Comparison of Bacterial Communities from Lava Cave Microbial Mats to Overlying Surface Soils from Lava Beds National Monument, USA. PLoS One, 12(2): e0169339. https://doi.org/10.1371/journal.pone.0169339

Lewin, G. R., Carlos, C., Chevrette, M. G., et al., 2016. Evolution and Ecology of Actinobacteria and Their Bioenergy Applications. Annual Review of Microbiology, 70: 235-254. https://doi.org/10.1146/annurev-micro-102215-095748

Lian, B., Xiao, L. L., Sun, Q. B., 2017. Ecological Effects of the Microbial Weathering of Silicate Minerals. Acta Geologica Sinica (English Edition), 91(Suppl. 1): 150-152. https://doi.org/10.1111/1755-6724.13231

Ma, L. Y., Huang, X. P., Wang, H. M., et al., 2021. Microbial Interactions Drive Distinct Taxonomic and Potential Metabolic Responses to Habitats in Karst Cave Ecosystem. Microbiology Spectrum, 9(2): e0115221. https://doi.org/10.1128/Spectrum.01152-21

Melillo, J. M., Frey, S. D., DeAngelis, K. M., et al., 2017. Long-Term Pattern and Magnitude of Soil Carbon Feedback to the Climate System in a Warming World. Science, 358(6359): 101-105. doi: 10.1126/science.aan2874

Morris, B. E. L., Henneberger, R., Huber, H., et al., 2013. Microbial Syntrophy: Interaction for the Common Good. FEMS Microbiology Reviews, 37(3): 384-406. https://doi.org/10.1111/1574-6976.12019

Mozafari, M., Sajjadian, M., Sorninia, Y., et al., 2020. Hydrogeology and Geomorphology of Bisetun Aquifer (NW Iran): Interesting Example of Deep Endokarst. Carbonates and Evaporites, 35(4): 1-19. https://doi.org/10.1007/s13146-020-00636-y

Nelson, M. B., Martiny, A. C., Martiny, J. B. H., 2016. Global Biogeography of Microbial Nitrogen-Cycling Traits in Soil. Proceedings of the National Academy of Sciences of the United States of America, 113(29): 8033-8040. https://doi.org/10.1073/pnas.1601070113

Ortiz, M., Legatzki, A., Neilson, J. W., et al., 2014. Making a Living While Starving in the Dark: Metagenomic Insights into the Energy Dynamics of a Carbonate Cave. The ISME Journal, 8(2): 478-491. https://doi.org/10.1038/ismej.2013.159

Poisot, T., Gravel, D., 2014. When is an Ecological Network Complex? Connectance Drives Degree Distribution and Emerging Network Properties. Peer Journal, 2: e251. https://doi.org/10.7717/peerj.251

Porter, M. L., Engel, A. S., Kane, T. C., et al., 2009. Productivity-Diversity Relationships from Chemolithoautotrophically Based Sulfidic Karst Systems. International Journal of Speleology, 38: 27-40. https://doi.org/10.5038/1827-806x.38.1.4

Pratscher, J., Vollmers, J., Wiegand, S., et al., 2018. Unravelling the Identity, Metabolic Potential and Global Biogeography of the Atmospheric Methane-Oxidizing Upland Soil Cluster α. Environmental Microbiology, 20(3): 1016-1029. https://doi.org/10.1111/1462-2920.14036

Proctor, L. M., 1997. Nitrogen-Fixing, Photosynthetic, Anaerobic Bacteria Associated with Pelagic Copepods. Aquatic Microbial Ecology, 12: 105-113. https://doi.org/10.3354/ame012105

Pu, G. Z., Lü, Y. N., Dong, L. N., et al., 2019. Profiling the Bacterial Diversity in a Typical Karst Tiankeng of China. Biomolecules, 9(5): 187. https://doi.org/10.3390/biom9050187

Puissant, J., Jones, B., Goodall, T., et al., 2019. The pH Optimum of Soil Exoenzymes Adapt to Long Term Changes in Soil pH. Soil Biology and Biochemistry, 138: 107601. https://doi.org/10.1016/j.soilbio.2019.107601

Radita, R., Suwanto, A., Kurosawa, N., et al., 2018. Firmicutes is the Predominant Bacteria in Tempeh. International Food Research Journal, 25(6): 2313-2320.

Reitschuler, C., Spötl, C., Hofmann, K., et al., 2016. Archaeal Distribution in Moonmilk Deposits from Alpine Caves and Their Ecophysiological Potential. Microbial Ecology, 71(3): 686-699. https://doi.org/10.1007/s00248-015-0727-z

Riquelme, C., Marshall Hathaway, J. J., de L N Enes Dapkevicius, M., et al., 2015. Actinobacterial Diversity in Volcanic Caves and Associated Geomicrobiological Interactions. Frontiers in Microbiology, 6: 1342. https://doi.org/10.3389/fmicb.2015.01342

Sauro, F., Mecchia, M., Tringham, M., et al., 2020. Speleogenesis of the World's Longest Cave in Hybrid Arenites (Krem Puri, Meghalaya, India). Geomorphology, 359: 107160. https://doi.org/10.1016/j.geomorph.2020.107160

Smit, E., Leeflang, P., Gommans, S., et al., 2001. Diversity and Seasonal Fluctuations of the Dominant Members of the Bacterial Soil Community in a Wheat Field as Determined by Cultivation and Molecular Methods. Applied and Environmental Microbiology, 67(5): 2284-2291. https://doi.org/10.1128/aem.67.5.2284-2291.2001

Sun, X. L., Xu, Z. H., Xie, J. Y., et al., 2022. Bacillus velezensis Stimulates Resident Rhizosphere Pseudomonas stutzeri for Plant Health through Metabolic Interactions. The ISME Journal, 16(3): 774-787. https://doi.org/10.1038/s31396-021-01125-3

Tang, K., Baskaran, V., Nemati, M., 2009. Bacteria of the Sulphur Cycle: An Overview of Microbiology, Biokinetics and Their Role in Petroleum and Mining Industries. Biochemical Engineering Journal, 44(1): 73-94. https://doi.org/10.1016/j.bej.2008.12.011

Tetu, S. G., Breakwell, K., Elbourne, L. D. H., et al., 2013. Life in the Dark: Metagenomic Evidence that a Microbial Slime Community is Driven by Inorganic Nitrogen Metabolism. The ISME Journal, 7(6): 1227-1236. https://doi.org/10.1038/ismej.2013.14

Veress, M. J., 2020. Karst Types and Their Karstification. Journal of Earth Science, 31(3): 621-634. https://doi.org/10.1007/s12583-020-1306-x

Wang, Q., Zhang, Z. H., Du, R., et al., 2019. Richness of Plant Communities Plays a Larger Role Than Climate in Determining Responses of Species Richness to Climate Change. Journal of Ecology, 107: 1944-1955. https://doi.org/10.1111/1365-2745.13148

Wang, W. F., Ma, Y. T., Ma, X., et al., 2012. Diversity and Seasonal Dynamics of Airborne Bacteria in the Mogao Grottoes, Dunhuang, China. Aerobiologia, 28(1): 27-38. https://doi.org/10.1007/s10453-011-9208-0

Wang, X. Y., He, T. H., Gen, S. Y., et al., 2020. Soil Properties and Agricultural Practices Shape Microbial Communities in Flooded and Rainfed Croplands. Applied Soil Ecology, 147: 103449. https://doi.org/10.1016/j.apsoil.2019.103449

Yang, S. H., Ahn, H., Kim, B. S., et al., 2017. Comparison of Bacterial Communities in Leachate from Decomposing Bovine Carcasses. Asian-Australasian Journal of Animal Sciences, 30(11): 1660-1666. https://doi.org/10.5713/ ajas.17.0553 doi: 10.5713/ajas.17.0553

Yang, Y., Li, T., Wang, Y. Q., et al., 2021. Linkage between Soil Ectoenzyme Stoichiometry Ratios and Microbial Diversity Following the Conversion of Cropland into Grassland. Agriculture, Ecosystems & Environment, 314: 107418. https://doi.org/10.1016/j.agee.2021.107418

Yun, Y. A., Wang, H. M., Man, B. Y., et al., 2016. The Relationship between pH and Bacterial Communities in a Single Karst Ecosystem and Its Implication for Soil Acidification. Frontiers in Microbiology, 7: 1955. https://doi.org/10.3389/fmicb.2016.01955

Yun, Y. A., Wang, W. Q., Wang, H. M., et al., 2018. Seasonal Variation of Bacterial Community and Their Functional Diversity in Drip Water from a Karst Cave. Chinese Science Bulletin, 63(36): 3932-3944. https://doi.org/10.1360/n972018-00627

Yun, Y. A., Xiang, X., Wang, H. M., et al., 2016. Five-Year Monitoring of Bacterial Communities in Dripping Water from the Heshang Cave in Central China: Implication for Paleoclimate Reconstruction and Ecological Functions. Geomicrobiology Journal, 33(7): 1-11. https://doi.org/10.1080/01490451.2015.1062062

Zelezniak, A., Andrejev, S., Ponomarova, O., et al., 2015. Metabolic Dependencies Drive Species Co-Occurrence in Diverse Microbial Communities. Proceedings of the National Academy of Sciences of the United States of America, 112(20): 6449-6454. https://doi.org/10.1073/pnas.1421834112

Zeng, L. L., Tian, J. Q., Chen, H., et al., 2019. Changes in Methane Oxidation Ability and Methanotrophic Community Composition across Different Climatic Zones. Journal of Soils and Sediments, 19(2): 533-543. https://doi.org/10.1007/s11368-018-2069-1

Zhang, Y., Yang, Q. S., Ling, J., et al., 2021. The Diversity of Alkane-Degrading Bacterial Communities in Seagrass Ecosystem of the South China Sea. Ecotoxicology, 30: 1799-1807. https://doi.org/10.1007/s10646-021-02450-1

Zhao, R., Wang, H. M., Cheng, X. Y., et al., 2018. Upland Soil Cluster γ Dominates the Methanotroph Communities in the Karst Heshang Cave. FEMS Microbiology Ecology, 94(12): fiy192. https://doi.org/10.1093/femsec/fiy192

Zhu, H. Z., Zhang, Z. F., Zhou, N., et al., 2019. Diversity, Distribution and Co-Occurrence Patterns of Bacterial Communities in a Karst Cave System. Frontiers in Microbiology, 10: 1726. https://doi.org/10.3389/fmicb.2019.01726

Zhu, H. Z., Zhang, Z. F., Zhou, N., et al., 2021. Bacteria and Metabolic Potential in Karst Caves Revealed by Intensive Bacterial Cultivation and Genome Assembly. Applied and Environmental Microbiology, 87(6): e02440-e02420. https://doi.org/10.1128/aem.02440-20

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