Temperature and Moisture Gradients Drive the Shifts of the Bacterial Microbiomes in 1000-Year-Old Mausoleums
Abstract
:1. Introduction
2. Materials and Methods
2.1. Sampling and Environmental Monitoring
2.2. DNA Isolation, PCR Conditions
2.3. Processing of High-Throughput Sequencing Data
2.4. Statistical Analysis
3. Results
3.1. The Hydrothermal Conditions in the Mausoleums
3.2. Bacterial Community Shifts and Their Driving Environmental Factors
3.3. Diversity of Bacterial Community
3.4. PICRUSt for Function Prediction
4. Discussion
4.1. Changing Patterns of Microbial Community along the Temperature and Moisture Gradients
4.2. Tourism-Related Activity Drives Microbial Community Shift
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Holden, C. Cave Paintings in Jeopardy. Science 2002, 297, 47. [Google Scholar] [CrossRef]
- Bastian, F.; Jurado, V.; Novakova, A.; Alabouvette, C.; Saiz-Jimenez, C. The microbiology of Lascaux Cave. Microbiology 2010, 156, 644–652. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cirigliano, A.; Mura, F.; Cecchini, A.; Tomassetti, M.C.; Maras, D.F.; Di Paola, M.; Meriggi, N.; Cavalieri, D.; Negri, R.; Quagliariello, A.; et al. Active microbial ecosystem in Iron-Age tombs of the Etruscan civilization. Environ. Microbiol. 2021, 23, 3957–3969. [Google Scholar] [CrossRef]
- Dakal, T.C.; Cameotra, S.S. Microbially induced deterioration of architectural heritages: Routes and mechanisms involved. Environ. Sci. Eur. 2012, 24, 36. [Google Scholar] [CrossRef] [Green Version]
- Scheerer, S.; Ortega-Morales, O.; Gaylarde, C. Microbial Deterioration of Stone Monuments—An Updated Overview. Adv. Appl. Microbiol. 2009, 66, 97–139. [Google Scholar] [CrossRef]
- Liu, X.; Koestler, R.J.; Warscheid, T.; Katayama, Y.; Gu, J.-D. Microbial deterioration and sustainable conservation of stone monuments and buildings. Nat. Sustain. 2020, 3, 991–1004. [Google Scholar] [CrossRef]
- Kakakhel, M.A.; Wu, F.; Gu, J.-D.; Feng, H.; Shah, K.; Wang, W. Controlling biodeterioration of cultural heritage objects with biocides: A review. Int. Biodeterior. Biodegrad. 2019, 143, 104721. [Google Scholar] [CrossRef]
- Caldeira, A.T.; Schiavon, N.; Mauran, G.; Salvador, C.; Rosado, T.; Mirão, J.; Candeias, A. On the Biodiversity and Biodeteriogenic Activity of Microbial Communities Present in the Hypogenic Environment of the Escoural Cave, Alentejo, Portugal. Coatings 2021, 11, 209. [Google Scholar] [CrossRef]
- Bartoli, F.; Municchia, A.C.; Futagami, Y.; Kashiwadani, H.; Moon, K.H.; Caneva, G. Biological colonization patterns on the ruins of Angkor temples (Cambodia) in the biodeterioration vs. bioprotection debate. Int. Biodeterior. Biodegrad. 2014, 96, 157–165. [Google Scholar] [CrossRef]
- Chen, J.; Gu, J.-D. The environmental factors used in correlation analysis with microbial community of environmental and cultural heritage samples. Int. Biodeterior. Biodegrad. 2022, 173, 105460. [Google Scholar] [CrossRef]
- Dakal, T.C.; Arora, P.K. Evaluation of potential of molecular and physical techniques in studying biodeterioration. Rev. Environ. Sci. Bio/Technol. 2012, 11, 71–104. [Google Scholar] [CrossRef]
- Nuhoglu, Y.; Oguz, E.; Uslu, H.; Ozbek, A.; Ipekoglu, B.; Ocak, I.; Hasenekoglu, I. The accelerating effects of the microorganisms on biodeterioration of stone monuments under air pollution and continental-cold climatic conditions in Erzurum, Turkey. Sci. Total Environ. 2006, 364, 272–283. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bontemps, Z.; Alonso, L.; Pommier, T.; Hugoni, M.; Moenne-Loccoz, Y. Microbial ecology of tourist Paleolithic caves. Sci. Total Environ. 2021, 816, 151492. [Google Scholar] [CrossRef] [PubMed]
- Mihajlovski, A.; Seyer, D.; Benamara, H.; Bousta, F.; Di Martino, P. An overview of techniques for the characterization and quantification of microbial colonization on stone monuments. Ann. Microbiol. 2014, 65, 1243–1255. [Google Scholar] [CrossRef] [Green Version]
- Soledad, C.; Sergio, S.M.; Cesareo, S.J.; Carlos, C.J. Microbial communities and associated mineral fabrics in Altamira Cave, Spain. Int. J. Speleol. 2009, 38, 83–92. [Google Scholar] [CrossRef] [Green Version]
- He, D.; Wu, F.; Ma, W.; Zhang, Y.; Gu, J.-D.; Duan, Y.; Xu, R.; Feng, H.; Wang, W.; Li, S.-W. Insights into the bacterial and fungal communities and microbiome that causes a microbe outbreak on ancient wall paintings in the Maijishan Grottoes. Int. Biodeterior. Biodegrad. 2021, 163, 105250. [Google Scholar] [CrossRef]
- Zhang, Y.; Wu, F.; Su, M.; He, D.; Gu, J.-D.; Guo, Q.; Kakakhel, M.A.; Yang, Y.; Wang, W.; Feng, H. Spatial and temporal distributions of microbial diversity under natural conditions on the sandstone stelae of the Beishiku Temple in China. Int. Biodeterior. Biodegrad. 2021, 163, 105279. [Google Scholar] [CrossRef]
- Ma, Y.; Zhang, H.; Du, Y.; Tian, T.; Xiang, T.; Liu, X.; Wu, F.; An, L.; Wang, W.; Gu, J.D.; et al. The community distribution of bacteria and fungi on ancient wall paintings of the Mogao Grottoes. Sci. Rep. 2015, 5, 7752. [Google Scholar] [CrossRef] [Green Version]
- Bastian, F.; Alabouvette, C. Lights and shadows on the conservation of a rock art cave: The case of Lascaux Cave. Int. J. Speleol. 2009, 38, 55–60. [Google Scholar] [CrossRef] [Green Version]
- Huang, Z.; Zhao, F.; Li, Y.; Zhang, J.; Feng, Y. Variations in the bacterial community compositions at different sites in the tomb of Emperor Yang of the Sui Dynasty. Microbiol. Res. 2017, 196, 26–33. [Google Scholar] [CrossRef]
- Ma, L.; Huang, X.; Wang, H.; Yun, Y.; Cheng, X.; Liu, D.; Lu, X.; Qiu, X. Microbial Interactions Drive Distinct Taxonomic and Potential Metabolic Responses to Habitats in Karst Cave Ecosystem. Microbiol. Spectr. 2021, 9, e0115221. [Google Scholar] [CrossRef] [PubMed]
- Wang, W.; Ma, X.; Ma, Y.; Mao, L.; Wu, F.; Ma, X.; An, L.; Feng, H. Seasonal dynamics of airborne fungi in different caves of the Mogao Grottoes, Dunhuang, China. Int. Biodeterior. Biodegrad. 2010, 64, 461–466. [Google Scholar] [CrossRef]
- Liu, X.; Meng, H.; Wang, Y.; Katayama, Y.; Gu, J.-D. Water is a critical factor in evaluating and assessing microbial colonization and destruction of Angkor sandstone monuments. Int. Biodeterior. Biodegrad. 2018, 133, 9–16. [Google Scholar] [CrossRef]
- Yao, S.; Yan, Z.; Ma, Q.; Xu, B.; Zhang, Z.; Bi, W.; Zhang, J. Analysis of the annual hygrothermal environment in the Maijishan Grottoes by field measurements and numerical simulations. Build. Environ. 2022, 221, 109229. [Google Scholar] [CrossRef]
- Zhu, H.Z.; Zhang, Z.F.; Zhou, N.; Jiang, C.Y.; Wang, B.J.; Cai, L.; Liu, S.J. Diversity, Distribution and Co-Occurrence Patterns of Bacterial Communities in a Karst Cave System. Front. Microbiol. 2019, 10, 1726. [Google Scholar] [CrossRef] [Green Version]
- Zerboni, A.; Villa, F.; Wu, Y.-L.; Solomon, T.; Trentini, A.; Rizzi, A.; Cappitelli, F.; Gallinaro, M. The Sustainability of Rock Art: Preservation and Research. Sustainability 2022, 14, 6305. [Google Scholar] [CrossRef]
- Mu, B.G.; Zhang, Y.; Yu, Y.J.; Petropoulos, E. Biomass Material Amendment Maintained the Structure of Underground Cultural Relics by Decreasing the Variation of Soil Water Content. Appl. Ecol. Environ. Res. 2022, 20, 801–814. [Google Scholar] [CrossRef]
- Liu, W.; Zhou, X.; Jin, T.; Li, Y.; Wu, B.; Yu, D.; Yu, Z.; Su, B.; Chen, R.; Feng, Y.; et al. Multikingdom interactions govern the microbiome in subterranean cultural heritage sites. Proc. Natl. Acad. Sci. USA 2022, 119, e2121141119. [Google Scholar] [CrossRef]
- Caporaso, J.G.; Kuczynski, J.; Stombaugh, J.; Bittinger, K.; Bushman, F.D.; Costello, E.K.; Fierer, N.; Pena, A.G.; Goodrich, J.K.; Gordon, J.I.; et al. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 2010, 7, 335–336. [Google Scholar] [CrossRef] [Green Version]
- Anderson, M.J.; Walsh, D.C.I. PERMANOVA, ANOSIM, and the Mantel test in the face of heterogeneous dispersions: What null hypothesis are you testing? Ecol. Monogr. 2013, 83, 557–574. [Google Scholar] [CrossRef]
- Revelle, W. psych: Procedures for Personality and Psychological Research, (R Package Version 1.3.2). Evanston, Illinois. 2017. Available online: https://www.scholars.northwestern.edu/en/publications/psych-procedures-for-personality-and-psychological-research (accessed on 27 November 2022).
- Koo, H.; Hakim, J.A.; Morrow, C.D.; Eipers, P.G.; Davila, A.; Andersen, D.T.; Bej, A.K. Comparison of two bioinformatics tools used to characterize the microbial diversity and predictive functional attributes of microbial mats from Lake Obersee, Antarctica. J. Microbiol. Methods 2017, 140, 15–22. [Google Scholar] [CrossRef] [PubMed]
- Valencia, E.; Gross, N.; Quero, J.L.; Carmona, C.P.; Ochoa, V.; Gozalo, B.; Delgado-Baquerizo, M.; Dumack, K.; Hamonts, K.; Singh, B.K.; et al. Cascading effects from plants to soil microorganisms explain how plant species richness and simulated climate change affect soil multifunctionality. Glob. Chang. Biol. 2018, 24, 5642–5654. [Google Scholar] [CrossRef] [PubMed]
- Kardol, P.; Cregger, M.A.; Campany, C.E.; Classen, A.T.J.E. Soil ecosystem functioning under climate change: Plant species and community effects. Ecology 2010, 91, 767–781. [Google Scholar] [CrossRef] [PubMed]
- Yao, M.; Rui, J.; Niu, H.; Heděnec, P.; Li, J.; He, Z.; Wang, J.; Cao, W.; Li, X. The differentiation of soil bacterial communities along a precipitation and temperature gradient in the eastern Inner Mongolia steppe. Catena 2017, 152, 47–56. [Google Scholar] [CrossRef]
- Li, J.; Deng, M.; Gao, L.; Yen, S.; Katayama, Y.; Gu, J.-D. The active microbes and biochemical processes contributing to deterioration of Angkor sandstone monuments under the tropical climate in Cambodia—A review. J. Cult. Herit. 2021, 47, 218–226. [Google Scholar] [CrossRef]
- Ding, X.; Lan, W.; Yan, A.; Li, Y.; Katayama, Y.; Gu, J.D. Microbiome characteristics and the key biochemical reactions identified on stone world cultural heritage under different climate conditions. J. Environ. Manag. 2022, 302, 114041. [Google Scholar] [CrossRef]
- Wu, F.; Zhang, Y.; He, D.; Gu, J.-D.; Guo, Q.; Liu, X.; Duan, Y.; Zhao, J.; Wang, W.; Feng, H. Community structures of bacteria and archaea associated with the biodeterioration of sandstone sculptures at the Beishiku Temple. Int. Biodeterior. Biodegrad. 2021, 164, 105290. [Google Scholar] [CrossRef]
- Frindte, K.; Pape, R.; Werner, K.; Loffler, J.; Knief, C. Temperature and soil moisture control microbial community composition in an arctic-alpine ecosystem along elevational and micro-topographic gradients. ISME J. 2019, 13, 2031–2043. [Google Scholar] [CrossRef]
- Li, Y.-H.; Gu, J.-D. A more accurate definition of water characteristics in stone materials for an improved understanding and effective protection of cultural heritage from biodeterioration. Int. Biodeterior. Biodegrad. 2022, 166, 105338. [Google Scholar] [CrossRef]
- Krakova, L.; De Leo, F.; Bruno, L.; Pangallo, D.; Urzi, C. Complex bacterial diversity in the white biofilms of the Catacombs of St. Callixtus in Rome evidenced by different investigation strategies. Environ. Microbiol. 2015, 17, 1738–1752. [Google Scholar] [CrossRef]
- Portillo, M.C.; Saiz-Jimenez, C.; Gonzalez, J.M. Molecular characterization of total and metabolically active bacterial communities of “white colonizations” in the Altamira Cave, Spain. Res. Microbiol. 2009, 160, 41–47. [Google Scholar] [CrossRef] [PubMed]
- Saarela, M.; Alakomi, H.L.; Suihko, M.L.; Maunuksela, L.; Raaska, L.; Mattila-Sandholm, T. Heterotrophic microorganisms in air and biofilm samples from Roman catacombs, with special emphasis on actinobacteria and fungi. Int. Biodeterior. Biodegrad. 2004, 54, 27–37. [Google Scholar] [CrossRef]
- Ai, J.; Guo, J.; Li, Y.; Zhong, X.; Lv, Y.; Li, J.; Yang, A. The diversity of microbes and prediction of their functions in karst caves under the influence of human tourism activities—A case study of Zhijin Cave in Southwest China. Environ. Sci. Pollut. Res. 2022, 29, 25858–25868. [Google Scholar] [CrossRef] [PubMed]
- Alonso, L.; Pommier, T.; Kaufmann, B.; Dubost, A.; Chapulliot, D.; Dore, J.; Douady, C.J.; Moenne-Loccoz, Y. Anthropization level of Lascaux Cave microbiome shown by regional-scale comparisons of pristine and anthropized caves. Mol. Ecol. 2019, 28, 3383–3394. [Google Scholar] [CrossRef]
- Farina, R.; Severi, M.; Carrieri, A.; Miotto, E.; Sabbioni, S.; Trombelli, L.; Scapoli, C. Whole metagenomic shotgun sequencing of the subgingival microbiome of diabetics and non-diabetics with different periodontal conditions. Arch. Oral Biol. 2019, 104, 13–23. [Google Scholar] [CrossRef]
- Ikner, L.A.; Toomey, R.S.; Nolan, G.; Neilson, J.W.; Pryor, B.M.; Maier, R.M. Culturable microbial diversity and the impact of tourism in Kartchner Caverns, Arizona. Microb. Ecol. 2007, 53, 30–42. [Google Scholar] [CrossRef] [PubMed]
- Zaura, E.; Keijser, B.J.; Huse, S.M.; Crielaard, W. Defining the healthy “core microbiome” of oral microbial communities. BMC Microbiol. 2009, 9, 259. [Google Scholar] [CrossRef] [Green Version]
- Mulec, J.; Oarga-Mulec, A.; Šturm, S.; Tomazin, R.; Matos, T. Spacio-Temporal Distribution and Tourist Impact on Airborne Bacteria in a Cave (Škocjan Caves, Slovenia). Diversity 2017, 9, 28. [Google Scholar] [CrossRef] [Green Version]
- Albertano, E.; Bruno, L. The importance of light in the conservation of hypogean monuments. In Proceedings of the International Congress on Molecular Biology and Cultural Heritage, Seville, Spain, 4–7 March 2003; pp. 171–177. [Google Scholar]
- Falasco, E.; Ector, L.; Isaia, M.; Wetzel, C.; Hoffmann, L.; Bona, F. Diatom flora in subterranean ecosystems: A review. Int. J. Speleol. 2014, 43, 231–251. [Google Scholar] [CrossRef] [Green Version]
- De Luca, D.; Caputo, P.; Perfetto, T.; Cennamo, P. Characterisation of Environmental Biofilms Colonising Wall Paintings of the Fornelle Cave in the Archaeological Site of Cales. Int. J. Environ. Res. Public Health 2021, 18, 8048. [Google Scholar] [CrossRef]
- Pfendler, S.; Karimi, B.; Maron, P.A.; Ciadamidaro, L.; Valot, B.; Bousta, F.; Alaoui-Sosse, L.; Alaoui-Sosse, B.; Aleya, L. Biofilm biodiversity in French and Swiss show caves using the metabarcoding approach: First data. Sci. Total Environ. 2018, 615, 1207–1217. [Google Scholar] [CrossRef] [PubMed]
- D’Angeli, I.M.; Serrazanetti, D.I.; Montanari, C.; Vannini, L.; Gardini, F.; De Waele, J. Geochemistry and microbial diversity of cave waters in the gypsum karst aquifers of Emilia Romagna region, Italy. Sci. Total Environ. 2017, 598, 538–552. [Google Scholar] [CrossRef] [PubMed]
- Mammola, S. Finding answers in the dark: Caves as models in ecology fifty years after Poulson and White. Ecography 2019, 42, 1331–1351. [Google Scholar] [CrossRef]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Li, X.; Zhou, X.; Wu, C.; Petropoulos, E.; Yu, Y.; Feng, Y. Temperature and Moisture Gradients Drive the Shifts of the Bacterial Microbiomes in 1000-Year-Old Mausoleums. Atmosphere 2023, 14, 14. https://doi.org/10.3390/atmos14010014
Li X, Zhou X, Wu C, Petropoulos E, Yu Y, Feng Y. Temperature and Moisture Gradients Drive the Shifts of the Bacterial Microbiomes in 1000-Year-Old Mausoleums. Atmosphere. 2023; 14(1):14. https://doi.org/10.3390/atmos14010014
Chicago/Turabian StyleLi, Xin, Xiao’ai Zhou, Chen Wu, Evangelos Petropoulos, Yongjie Yu, and Youzhi Feng. 2023. "Temperature and Moisture Gradients Drive the Shifts of the Bacterial Microbiomes in 1000-Year-Old Mausoleums" Atmosphere 14, no. 1: 14. https://doi.org/10.3390/atmos14010014