Skip to content
Licensed Unlicensed Requires Authentication Published by De Gruyter March 15, 2018

Analysis of the bacterial communities in the waterlogged wooden cultural relics of the Xiaobaijiao No. 1 shipwreck via high-throughput sequencing technology

  • Qiuxia Li , Lixiang Cao , Wenfeng Wang , Hongming Tan , Tao Jin , Guangyuan Wang , Guocong Lin and Runlin Xu EMAIL logo
From the journal Holzforschung

Abstract

The microbial impact on waterlogged wooden cultural relics from Xiaobaijiao No. 1 shipwreck was investigated by means of a high-throughput sequencing technology, while the focus was on the composition of prokaryotic microorganisms in 10 wood samples collected from different parts of the shipwreck. A total of 28 501 different operational taxonomic units (OTUs) were obtained based on 97% sequence similarity. The α-diversity index is for the bacterial diversity, which was the highest and the lowest in the samples SS8 and SS5, respectively. Proteobacteria was the largest category of bacterial abundance (47.3%) followed by Bacteroidetes (10%). α-Proteobacteria was the first largest bacteria class with the maximum abundance (21.0%) followed by γ-Proteobacteria (16.9%). Other groups rich in the following species were found: Bacteroidales (13.3%), Thiotrichales (5.0%), Rhodobacterales (4.2%), Rhizobiales (4.0%), Chromatiales (3.5%), Oceanospirillales (3.3%), Flavobacteriales (2.9%) and Sphingomonadales (2.8%). At the level of the bacterial genus, Marinomonas was the most abundant one. Phylogenetic analysis revealed that there are some differences in the composition of bacterial communities from different wood samples. The species number of bacteria in the relics of this shipwreck was far more than that reported in those found in Europe, and in which species composition was similar to the benthic bacteria in the corresponding sea area. The coexistence of anaerobic and aerobic bacteria is remarkable.

Acknowledgments

This work was funded by the special research project of underwater heritage protection from the State Administration of Cultural Heritage of China (Project no.: 2013-538).

  1. Author contributions: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.

  2. Research funding: The special research project of underwater heritage protection from the State Administration of Cultural Heritage of China (Project No.: 2013-538).

  3. Employment or leadership: None declared.

  4. Honorarium: None declared.

References

Almkvist, G., Persson, I. (2008a) Analysis of acids and degradation products related to iron and sulfur in the Swedish warship Vasa. Holzforschung 62:694–703.10.1515/HF.2008.130Search in Google Scholar

Almkvist, G., Persson, I. (2008b) Degradation of polyethylene glycol and hemicellulose in the Vasa. Holzforschung 62:64–70.10.1515/HF.2008.009Search in Google Scholar

Almkvist, G., Norbakhsh, S., Bjurhager, I., Varmuza, K. (2016) Prediction of tensile strength in iron-contaminated archaeological wood by FT-IR spectroscopy – a study of degradation in recent oak and Vasa oak. Holzforschung 70:855–865.10.1515/hf-2015-0223Search in Google Scholar

Amann, R.I., Ludwig, W., Sehleifer, K.H. (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol. Rev. 59:143–169.10.1128/mr.59.1.143-169.1995Search in Google Scholar

Amin, S.A., Green, D.H., Waheeb, A.D., Gärdes, A., Carrano, C.J. (2012) Iron transport in the genus Marinobacter. Biometals 25:135–147.10.1007/s10534-011-9491-9Search in Google Scholar

Björdal, C.G. (2012) Evaluation of the microbial degradation of shipwreck in the Baltic Sea. Rev. Int. Biodeter. Biodegr. 70:126–140.10.1016/j.ibiod.2012.01.012Search in Google Scholar

Björdal, C.G., Nilsson, T., Daniel, G. (1999) Microbial decay of waterlogged wood found in Sweden applicable to archaeology and conservation. Int. Biodeter. Biodegr. 43:63–73.10.1016/S0964-8305(98)00070-5Search in Google Scholar

Bjurhager, I., Ljungdahl, J., Wallström, L., Gamstedt, E.K., Berglund, L.A. (2010) Towards improved understanding of PEG-impregnated waterlogged archaeological wood: a model study on recent oak. Holzforschung 64:243–250.10.1515/hf.2010.024Search in Google Scholar

Bokulich, N.A., Subramanian, S., Faith, J.J., Gevers, D., Gordon, J.I., Knight, R., Mills, D.A., Caporaso, J.G. (2013) Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nat. Methods 10:57–59.10.1038/nmeth.2276Search in Google Scholar PubMed PubMed Central

Caporaso, J.G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F.D.E., Costello, K., Fierer, N., Peña, A.G., Goodrich, J.K., Gordon, J.I., Huttley, G.A., Kelley, S.T. (2010) QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7:335–336.10.1038/nmeth.f.303Search in Google Scholar PubMed PubMed Central

Daniel, G.F., Nilsson, T., Singh, A.P. (1989) Degradation of lignocellulosics by unique tunnel-forming bacteria. Can. J. Microbiol. 33:943–948.10.1139/m87-166Search in Google Scholar

Degnan, P.H., Ochman, H. (2012) Illumina-based analysis of microbial community diversity. ISME J. 6:183–194.10.1038/ismej.2011.74Search in Google Scholar PubMed PubMed Central

Edgar, R.C. (2013) UPARSE: highly accurate OTU sequences from microbial ampliconreads. Nat. Methods 10:996–998.10.1038/nmeth.2604Search in Google Scholar PubMed

Fandino, L.B., Riemann, L., Steward, G.F., Azam, F. (2005) Population dynamics of Cytophaga-Flavobacteria during marine phytoplankton blooms analyzed by real-time quantitative PCR. Aquat. Microb. Ecol. 40:251–257.10.3354/ame040251Search in Google Scholar

Feng, B.W., Li, X.R., Wang, J.H., Hu, Z.Y., Meng, H., Xiang, L.Y., Quan, Z.X. (2009) Bacterial diversity of water and sediment in the Changjiang estuary and coastal area of the East China Sea. FEMS Microbiol. Ecol. 70:236–248.10.1111/j.1574-6941.2009.00772.xSearch in Google Scholar PubMed

Feng, X.X., Gao, M.G., Jin, T., Lin, G.G., Xu, R.L. (2017) Supplementary identification of wood species from the Qing Dynasty shipwreck “Xiaobaijiao 1” in Ningbo. Sci. Conserv. Archaeol. 29:72–77.Search in Google Scholar

Finster, K. (2011) Microbiological disproportion at ion of inorganic sulfur compounds. J. Sulfur Chem. 2144:281–292.Search in Google Scholar

Florian, M.L. (1987) Deterioration of organic materials other than wood. In: Conservation of Marine Archaeological Objects. Ed. Pearson, C. Butterworths, London. pp. 21–54.10.1016/B978-0-408-10668-9.50008-3Search in Google Scholar

Fors, Y. (2014) Sulfur-related conservation concerns for marine archaeological wood: the origin, speciation and distribution of accumulated sulfur with some remedies for the Vasa. Doctoral Thesis of Stockholm University.Search in Google Scholar

Fors, Y., Sandström, M. (2006) Sulfur and iron in shipwrecks cause conservation concerns. Chem. Soc. Rev. 35:399–415.10.1039/b507010bSearch in Google Scholar PubMed

Gao, M.G., Zhang, Q.F., Jin, T., Luo, P., Li, Q., Xu, R.L. (2017) Observation and damage assessment of microbial diseases in some wooden cultural relics from the ancient marine shipwreck, Ningbo “Xiaobaijiao No. 1”. Sci. Conserv. Archaeol. 29:93–102.Search in Google Scholar

Guo, J.L., Fan, J.F., Fu, H. (2013) Analysis of the bacterial diversity in the sediments of Shuang Taizi estuary. Microbiol. China 40:1550–1559.Search in Google Scholar

Haas, B.J., Gevers, D., Earl, A.M., Feldgarden, M., Ward, D.V., Giannoukos, G., Ciulla, D., Tabbaa, D., Highlander, S.K., Sodergren, E., Methé, B., DeSantis, T.Z., Petrosino, J.F., Knight, R., Birren, B.W. (2011) Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Res. 21:494–504.10.1101/gr.112730.110Search in Google Scholar PubMed PubMed Central

Helms, A.C., Martiny, A.C., Hofman-Bang, J.B., Ahring, K., Kilstrup, M. (2004) Identification of bacterial cultures from archaeological wood using molecular biological techniques. Int. Biodeter. Biodegr. 53:79–88.10.1016/j.ibiod.2003.10.003Search in Google Scholar

Hoffmann, P. (1988) On the stabilization of waterlogged oakwood with polyethylene glycol (PEG) III. Testing the oligomers. Holzforschung 42:289–294.10.1515/hfsg.1988.42.5.289Search in Google Scholar

Holt, D.M. (1983) Bacterial degradation of lignified wood cell walls in aerobic aquatic habitats: decay patterns and mechanisms proposed to account for their formation. J. Inst. Wood Sci. 9:212–223.Search in Google Scholar

Holt, D.M., Jones, E.B.G. (1983) Bacterial degradation of lignified wood cell walls in anaerobic aquatic habitats. Appl. Environ. Microbiol. 46:722–727.10.1128/aem.46.3.722-727.1983Search in Google Scholar PubMed PubMed Central

Jiang, R., Wang, J.X., Huang, B., Zhang, P., Zhen, J.W., Yu, K.C., Liu, M.H. (2015) Bacterial diversity in sediments in Jiaojiang River estuary. Oceanol. Limnol. Sin. 46:887–900.Search in Google Scholar

Jin, T., Li, N.S. (2016) Investigation of the deterioration and evaluation of the status of the hull of the “Xiaobaijiao 1” shipwreck. Ningbo. Sci. Conserv. Archaeol. 28:93–100.Search in Google Scholar

Jin, T., Lin, G.C., Wang, G.Y. (2015) Identification of tree species and of timbers on the Qing Dynasty “Xiaobaijiao 1” shipwreck found in Xiangshan, Ningbo, Zhejiang. Sci. Conserv. Archaeol. 27:34–39.Search in Google Scholar

Jin, T., Ruan, X., Chen, J.W. (2016) Study of underwater burial environment of Ningbo “Xiaobaijiao l” shipwreck and its impact. Chin. Cult. Herit. Sci. Res. 1:59–62.Search in Google Scholar

Kato, S., Haruta, S., Cui, Z.J., Ishii, M., Igarashi, Y. (2004) Effective cellulose degradation by a mixed-culture system composed of a cellulolytic Clostridium and aerobic non-cellulolytic bacteria. FEMS Microbiol. Ecol. 51:133–142.10.1016/j.femsec.2004.07.015Search in Google Scholar PubMed

Kelly, D.P., Wood, A.P. (2000) Reclassification of some species of Thiobacillus to the newly designated genera Acidithiobacillus gen. nov., Halothiobacillus gen. nov. and Thermithiobacillus gen. nov. Int. J. Syst. Evol. Microbiol. 50:511–516.10.1099/00207713-50-2-511Search in Google Scholar PubMed

Kim, Y.S., Singh, A.P. (2016) Wood as cultural heritage material and its deterioration by biotic and abiotic agents. In: Secondary Xylem Biology: Origins, Functions, and Applications. Eds. Kim, Y.S., Funada, R., Singh, A.P. Elsevier, Amsterdam. pp. 233–257.10.1016/B978-0-12-802185-9.00012-7Search in Google Scholar

Klaassen, R.K.W.M. (2008) Bacterial decay in wooden foundation pile-patterns and causes: a study of historical pile foundations in the Netherlands. Int. Biodeter. Biodegr. 61:45–60.10.1016/j.ibiod.2007.07.006Search in Google Scholar

Kõljalg, U., Nilsson, R.H., Abarenkov, K., Tedersoo, L., Taylor, A.F.S., Bahram, M. (2013) Towards a unified paradigm for sequence-based identification of fungi. Mol. Ecol. 22:5271–5277.10.1111/mec.12481Search in Google Scholar PubMed

Landy, E.T., Mitchell, J.I., Hotchkiss, S., Eaton, R.A. (2008) Bacterial diversity associated with archaeological waterlogged wood: ribosomal RNA clone libraries and denaturing gradient gel electrophoresis (DGGE). Int. Biodeter. Biodegr. 61:106–116.10.1016/j.ibiod.2007.07.007Search in Google Scholar

Lin, G.C., Wang, G.Y., Jin, T. (2015) A brief excavation report in 2012 on the sunken ship in Qing Dynasty in Xiangshan County, Zhejiang. Archaeology 6:54–67.Search in Google Scholar

Magoč, T., Salzberg, S.L. (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963.10.1093/bioinformatics/btr507Search in Google Scholar PubMed PubMed Central

Mitchell, R., Gu, J.D. Environmental Microbiology, 2nd ed. Wiley-Blackwell, Hoboken, 2010.Search in Google Scholar

Nilsson, T., Björdal, C.G., Fallma, E. (2008) Culturing erosion bacteria: procedures for obtaining pure culture. Int. Biodeter. Biodegr. 61:17–23.10.1016/j.ibiod.2007.06.010Search in Google Scholar

Nogi, Y., Hosoya, S., Kato, C., Horikoshi, K. (2007) Psychromonas hadalis sp. nov., a novel piezophilic bacterium isolated from the bottom of the Japan Trench. Int. J. Syst. Evol. Microbiol. 57:1360–1364.10.1099/ijs.0.64933-0Search in Google Scholar PubMed

Preston, J., Watts, J.E.M., Jones, M. (2012) Novel bacterial community associated with 500-year-old unpreserved archaeological wood from King Henry VIII’s tudor warship the Mary Rose. Appl. Environ. Microbiol. 78:8822–8828.10.1128/AEM.02387-12Search in Google Scholar PubMed PubMed Central

Ondov, B.D.N., Bergman, H.A., Phillippy, M. (2011) Interactive metagenomic visualization in a Web browser. BMC Bioinformatics 12:385–394.10.1186/1471-2105-12-385Search in Google Scholar PubMed PubMed Central

Sandström, M., Jalilehvand, F., Persson, I., Gelius, U., Frank, P., Hall-Roth, I. (2002) Deterioration of the seventeenth-century warship Vasa by internal formation of sulphuric acid. Nature 415:893–897.10.1038/415893aSearch in Google Scholar PubMed

Sandström, M., Jalilehvand, F., Damian, E., Fors, Y., Gelius, U., Jones, M., Salome, M. (2005) Sulfur accumulation in the timbers of King Henry VIII’s warship Mary Rose: a pathway in the sulfur cycle of conservation concern. Proc. Natl. Acad. Sci. 102:14165–14170.10.1073/pnas.0504490102Search in Google Scholar PubMed PubMed Central

Singh, A.P. (2012) A review of microbial decay types found in wooden objects of cultural heritage recovered from buried and waterlogged environments. J. Cult. Herit. 13S: S16–S20.10.1016/j.culher.2012.04.002Search in Google Scholar

Singh, A.P., Kim, Y.S., Wi, S.G., Lee, K.H., Kim, I.J. (2003) Evidence of the degradation of middle lamella in a waterlogged archaeological wood. Holzforschung 57:115–119.10.1515/HF.2003.018Search in Google Scholar

Svedström, K., Bjurhager, I., Kallonen, A., Peura, M., Serimaa, R. (2012) Structure of oak wood from the Swedish warship Vasa revealed by X-ray scattering and microtomography. Holzforschung 66:355–363.10.1515/hf.2011.157Search in Google Scholar

Tortora, G.J., Funke, B.R., Case, C.L. Microbiology: An Introduction, 10th ed. Benjamin Cummings, San Francisco, 2010.Search in Google Scholar

Uthick, S., McGuire, K. (2007) Bacterial communities in barrier reef calcareous sediments: contrasting 16S rDNA libraries from near shore and outer shelf reefs. Estuar. Coast. Shelf Sci. 72:188–200.10.1016/j.ecss.2006.10.017Search in Google Scholar

Vorobyev, A., Arnould, O., Laux, D., Longo, R., van Dijk, N.P., Gamstedt, E.K. (2016) Characterisation of cubic oak specimens from the Vasa ship and recent wood by means of quasi-static loading and resonance ultrasound spectroscopy (RUS). Holzforschung 70:457–465.10.1515/hf-2015-0073Search in Google Scholar

Vorobyev, A., Almkvist, G., van Dijk, N.P., Gamstedt, E.K. (2017) Relations of density, polyethylene glycol treatment and moisture content with stiffness properties of Vasa oak samples. Holzforschung 71:327–335.10.1515/hf-2016-0202Search in Google Scholar

Wang, X.X. Bacterial Diversity in Sedimentary Environment of the Yangtze Estuary and East China Sea and Degradation of PAHs in the Western Pacific Ocean. Ocean University of China, Qingdao, 2008.Search in Google Scholar

Wang, Q., Garrity, G.M., Tiedje, J.M., Cole, J.R. (2007) Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73:5261–5267.10.1128/AEM.00062-07Search in Google Scholar PubMed PubMed Central

Wang, J.X., Xu, X.N., Zhou, L.L. (2012) A preliminary study of microbial diversity of the surface layer sediments from the East China Sea. Oceanol. Limnol. Sin. 43:805–813.Search in Google Scholar

Wang, Z.H., Xu, M.Q., Xie, L., Zhang, D.J., Zhou, J., He, W.N., Chen, L.P., Tong, Q.Q., Zhang, C.D., Su, X.R. (2014) Distribution of Bacteroidetes in Ningbo coastal sewage outlets. Oceanol. Limnol. Sin. 45:1030–1036.Search in Google Scholar

Wetherall, K.M., Moss, R.M., Jones, A.M., Smith, A.D., Skinner, T., Pickup, D.M., Newport, R.J. (2008) Sulfur and iron speciation in recently recovered timbers of the Mary Rose revealed via X-ray absorption spectroscopy. J. Archaeol. Sci. 35:1317–1328.10.1016/j.jas.2007.09.007Search in Google Scholar

Ye, J.Y., Luo, G.Y. (2004) Progress in biodiversity of nonculturable microorganisms and microbial molecular ecology. Microbiol. China 31:111–115.Search in Google Scholar

Zhao, X.R., Lin, Q.M., Sun, Y.X., Wang, Y.S., Zhang, Y.S., Zhang, M.Q. (2000) Decompostion of different cellulose materials by some cellulose-decomposing microbes. J. Micrbiol. 20:12–14.Search in Google Scholar

Received: 2017-08-23
Accepted: 2018-02-14
Published Online: 2018-03-15
Published in Print: 2018-07-26

©2018 Walter de Gruyter GmbH, Berlin/Boston

Downloaded on 1.12.2023 from https://www.degruyter.com/document/doi/10.1515/hf-2017-0132/pdf
Scroll to top button