Skip to content
Licensed Unlicensed Requires Authentication Published by De Gruyter April 26, 2022

Bacterial decay in waterlogged archaeological compression wood varies with severity of compression wood

  • Jong Sik Kim ORCID logo EMAIL logo , Mi Young Cha , Kwang Ho Lee and Yoon Soo Kim
From the journal Holzforschung

Abstract

Bacterial decay in compression wood (CW) tracheids of waterlogged archaeological wood (WAW) was investigated using light microscopy, confocal laser scanning microscopy, transmission electron microscopy (TEM), and TEM immunogold labeling. Erosion bacteria were identified as the main degraders, and the extent of cell wall degradation differed depending on the severity of CW tracheids (mild vs. severe). Mild CW tracheids showed preferential decay in the inner S2 layer, with the locally degraded and/or fragmented S3 layer remaining. In contrast, severe CW tracheids revealed gradual degradation of the cell wall from the erosion progressing from exposed faces of the cell wall as decay progressed. The overall decay was more extensive in mild than in severe CW tracheids, and degradation of the highly lignified outer S2 layer (S2L) was only detected in mild CW tracheids. TEM immunogold labeling of 1,4-β-galactan, homogalacturonan (HG), heteroxylan, and heteromannan epitopes showed that there was no preferential degradation of pectins and hemicelluloses by action of diffusible enzymes and/or agents through the un-decayed cell wall during bacterial decay, in both mild and severe CW tracheids. Inter-CW tracheid bordered pit membranes showed higher decay resistance than CW tracheid walls. Degradation of HG and heteromannan epitopes was suppressed in pit membranes.


Corresponding author: Jong Sik Kim, Department of Wood Science and Engineering, Chonnam National University, Gwangju 61186, Republic of Korea, E-mail:

Award Identifier / Grant number: NRF-2021R1F1A1063024

Acknowledgements

The authors gratefully acknowledge the National Research Institute of Maritime Cultural Heritage in the Republic of Korea for providing us with the Daebudo shipwreck no. 2 sample.

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

  2. Research funding: This work was supported by the National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIT) (no. NRF-2021R1F1A1063024).

  3. Conflict of interest statement: The authors declare no conflicts of interest regarding this article.

References

Altaner, C., Hapca, A.I., Knox, J.P., and Jarvis, M.C. (2007). Detection of ß-1–4-galactan in compression wood of Sitka spruce [Picea sitchensis (Bong.) Carriére] by immunofluorescence. Holzforschung 61: 311–316. https://doi.org/10.1515/hf.2007.049.Search in Google Scholar

Arantes, V., Jellison, J., and Goodell, B. (2012). Peculiarities of brown-rot fungi and biochemical Fenton reaction with regard to their potential as a model for bioprocessing biomass. Appl. Microbiol. Biotechnol. 94: 323–338. https://doi.org/10.1007/s00253-012-3954-y.Search in Google Scholar

Björdal, C.G. (2000). Waterlogged archaeological wood: biodegradation and its implications for conservation, Ph.D. thesis. Uppsala, Swedish University of Agricultural Sciences.Search in Google Scholar

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

Björdal, C.G., Daniel, G., and Nilsson, T. (2000). Depth of burial, an important factor in controlling bacterial decay of waterlogged archaeological poles. Int. Biodeterior. Biodegrad. 45: 15–26.10.1016/S0964-8305(00)00035-4Search in Google Scholar

Blanchette, R.A., Obst, J.R., and Timell, T.E. (1994). Biodegradation of compression wood and tension wood by white and brown rot fungi. Holzforschung 48: 34–42. https://doi.org/10.1515/hfsg.1994.48.s1.34.Search in Google Scholar

Cha, M.Y., Lee, K.H., Kim, J.S., and Kim, Y.S. (2021). Variations in bacterial decay between cell types and between cell wall regions in waterlogged archaeological wood excavated in the intertidal zone. IAWA J. 42: 457–474. https://doi.org/10.1163/22941932-bja10068.Search in Google Scholar

Curling, S.F., Clausen, C.A., and Winandy, J.E. (2002). Relationship between mechanical properties, weight loss and chemical composition of wood during incipient brown-rot decay. For. Prod. J. 52: 34–39.Search in Google Scholar

Côté, W.A.Jr., Timell, T.E., and Zabel, R.A. (1966). Distribution of lignin in compression wood of red spruce (Picea rubens Sarg.). Holz als Roh- Werkst. 24: 432–438.10.1007/BF02612868Search in Google Scholar

Côté, W.A.Jr., Pickard, P.A., and Timell, T.E. (1967). Studies on compression wood. IV. Fractional extraction and preliminary characterization of polysaccharides in normal and compression wood of Balsam fir. TAPPI (Tech. Assoc. Pulp Pap. Ind.) 50: 350–356.Search in Google Scholar

Daniel, G. (2003). Microview of wood under degradation by bacteria and fungi. In:Goodell, B., Nicholas, D.D., and Schultz, T.P. (Eds.), Wood deterioration and preservation. ACS Publications, Washington, DC, pp. 34–72. https://doi.org/10.1021/bk-2003-0845.ch004.Search in Google Scholar

Daniel, G. (2016). Fungal degradation of wood cell walls. In:Kim, Y.S., Funada, R., and Singh, A.P. (Eds.), Secondary xylem biology. Academic Press, London, pp. 131–167.https://doi.org/10.1016/b978-0-12-802185-9.00008-5.Search in Google Scholar

Daniel, G. and Nilsson, T. (1986). Ultrastructural observations on wood-degrading erosion bacteria. In: Proceedings of the International Research Group on Wood Preservation, Avognon, France. Document No. IRG/WP/1283.Search in Google Scholar

Donaldson, L.A. and Knox, J.P. (2012). Localization of cell wall polysaccharides in normal and compression wood of radiata pine: relationships with lignification and microfibril orientation. Plant Physiol. 158: 642–653. https://doi.org/10.1104/pp.111.184036.Search in Google Scholar PubMed PubMed Central

Donaldson, L.A., Singh, A.P., Yoshinaga, A., and Takabe, K. (1999). Lignin distribution in mild compression wood of Pinus radiata. Can. J. Bot. 77: 41–50. https://doi.org/10.1139/b98-190.Search in Google Scholar

Donaldson, L.A., Grace, J., and Downes, G.M. (2004). Within-tree variation in anatomical properties of compression wood in radiata pine. IAWA J. 25: 350–356. https://doi.org/10.1163/22941932-90000364.Search in Google Scholar

Fukushima, K. and Terashima, N. (1991). Heterogeneity in formation of lignin. Part XV: formation and structure of lignin in compression wood of Pinus thunbergii studied by microautoradiography. Wood Sci. Technol. 25: 371–381. https://doi.org/10.1007/bf00226177.Search in Google Scholar

Goodell, B., Jellison, J., Liu, J., Daniel, G., Paszczynski, A., Fekete, F., Krishnamurthy, S., Jun, L., and Xu, G. (1997). Low molecular weight chelators and phenolic compounds isolated from wood decay fungi and their role in the fungal biodegradation of wood. J. Biotechnol. 53: 133–162. https://doi.org/10.1016/s0168-1656(97)01681-7.Search in Google Scholar

Hoffmann, G.C. and Timell, T.E. (1972a). Polysaccharides in compression wood of tamarack (Larix laricina). 2. Isolation and structure of a xylan. Svensk Paperstidn 75: 241–242.Search in Google Scholar

Hoffmann, G.C. and Timell, T.E. (1972b). Polysaccharides in compression wood of tamarack (Larix laricina). 3. Constitution of a galactoglucomannan. Svensk Paperstidn 75: 297–298.Search in Google Scholar

Jones, L., Seymour, G.B., and Knox, J.P. (1997). Localization of pectic galactan in tomato cell walls using a monoclonal antibody specific to (1→4)-β-ᴅ-galactan. Plant Physiol. 113: 1405–1412. https://doi.org/10.1104/pp.113.4.1405.Search in Google Scholar PubMed PubMed Central

Kim, J.S. and Daniel, G. (2012). Distribution of glucomannans and xylans in poplar xylem and their changes under tension stress. Planta 236: 35–50. https://doi.org/10.1007/s00425-012-1588-z.Search in Google Scholar PubMed

Kim, J.S., Awano, T., Yoshinaga, A., and Takabe, K. (2010). Immunolocalization of ß-1–4-galactan and its relationship with lignin distribution in developing compression wood of Cryptomeria japonica. Planta 232: 109–119. https://doi.org/10.1007/s00425-010-1152-7.Search in Google Scholar PubMed

Kim, J.S., Awano, T., Yoshinaga, A., and Takabe, K. (2012). Occurrence of xylan and mannan polysaccharides and their spatial relationship with other cell wall components in differentiating compression wood tracheids of Cryptomeria japonica. Planta 233: 721–735. https://doi.org/10.1007/s00425-010-1333-4.Search in Google Scholar PubMed

Kim, J.S., Gao, J., and Daniel, G. (2015). Ultrastructure and immunocytochemistry of degradation in spruce and ash sapwood by the brown rot fungus Postia placenta: characterization of incipient stages of decay and variation in decay process. Int. Biodeterior. Biodegrad. 103: 161–178. https://doi.org/10.1016/j.ibiod.2015.05.005.Search in Google Scholar

Kim, Y.S. (2017). Micromorphological and chemical characteristics of waterlogged archaeological Yunnan pines (Pinus yunnanensis). J. Natl. Acad. Sci. Repub. Korea Nat. Sci. Ser. 56: 225–249, (Text in Korean). https://doi.org/10.5656/ksae.2017.05.0.001.Search in Google Scholar

Kim, Y.S. and Singh, A.P. (1999). Micromorphological characteristics of compression wood degradation in waterlogged archaeological pine wood. Holzforschung 63: 381–385. https://doi.org/10.1515/hf.1999.063.Search in Google Scholar

Kim, Y.S., Choi, J.H., Bae, H.J., Nilsson, T., and Daniel, G. (1992). Ultrastructural observation of bacterial attacks on the waterlogged archaeological woods. J. Conserv. Sci. 1: 3–11, (Text in Korean).Search in Google Scholar

Kim, Y.S., Singh, A.P., and Nilsson, T. (1996). Bacteria as important degraders in waterlogged archaeological woods. Holzforschung 50: 389–392. https://doi.org/10.1515/hfsg.1996.50.5.389.Search in Google Scholar

Marcus, S., Blake, A.W., Benians, T.A.S., Lee, K.J.D., Poyser, C., Donaldson, L., Leroux, O., Rogowski, A., Petersen, H.L., Boraston, A., et al.. (2010). Restricted access of proteins to mannan polysaccharides in intact plant cell walls. Plant J. 64: 191–203. https://doi.org/10.1111/j.1365-313x.2010.04319.x.Search in Google Scholar PubMed

McCartney, L., Marcus, S.E., and Knox, J.P. (2005). Monoclonal antibodies to plant cell wall xylans and arabinoxylans. J. Histochem. Cytochem. 53: 543–546. https://doi.org/10.1369/jhc.4b6578.2005.Search in Google Scholar PubMed

Nam, T.G., Yoon, Y.H., and Kim, E.H. (2018). Species identification and radiocarbon dating for the wooden board from Daebudo shipwreck No.2 using wiggle matching. J. Conserv. Sci. 34: 359–368, (Text in Korean). https://doi.org/10.12654/jcs.2018.34.5.04.Search in Google Scholar

Nanayakkara, B., Manley-Harris, M., Suckling, I.D., and Donaldson, L.A. (2009). Quantitative chemical indicators to assess the gradation of compression wood. Holzforschung 63: 431–439. https://doi.org/10.1515/hf.2009.062.Search in Google Scholar

National Research Institute of Maritime Cultural Heritage of Korea (2016). Ansan Daebudo shipwreck no.2 – Underwater excavation (Government publications registration No. 11-1550197-000051-01). Mokpo, Republic of Korea.Search in Google Scholar

Pedersen, N.B., Schmitt, U., Koch, G., Felby, C., and Garbrecht, T. (2014). Lignin distribution in waterlogged archaeological Picea abies (L.) Karst degraded by erosion bacteria. Holzforschung 68: 791–798. https://doi.org/10.1515/hf-2013-0228.Search in Google Scholar

Pedersen, N.B., Gierlinger, N., and Thygesen, L.G. (2015). Bacterial and abiotic decay in waterlogged archaeological Picea abies (L.) Karst studied by confocal Raman imaging and ATR-FTIR spectroscopy. Holzforschung 69: 103–112. https://doi.org/10.1515/hf-2014-0024.Search in Google Scholar

Rehbein, M., Koch, G., Schmitt, U., and Huckfeldt, T. (2013). Topochemical and transmission electron microscopic studies of bacterial decay in pine (Pinus sylvestris L.) harbour foundation piles. Micron 44: 150–158. https://doi.org/10.1016/j.micron.2012.05.012.Search in Google Scholar PubMed

Schmitt, U., Singh, A.P., Thieme, H., Friedrich, P., and Hoffmann, P. (2005). Electron microscopic characterization of cell wall degradation of the 400,000-year-old wooden Schöningen spears. Holz als Roh- Werkst. 63: 118–122. https://doi.org/10.1007/s00107-004-0542-6.Search in Google Scholar

Singh, A.P. (1997a). The ultrastructure of the attack of Pinus radiata mild compression wood by erosion and tunneling bacteria. Can. J. Bot. 75: 1095–1102. https://doi.org/10.1139/b97-120.Search in Google Scholar

Singh, A.P. (1997b). Initial pit borders in Pinus radiata are resistant to degradation by soft rot fungi and erosion bacteria but not tunneling bacteria. Holzforschung 51: 15–18.Search in Google Scholar

Singh, A.P. and Donaldson, L. (1999). Ultrastructure of tracheid cell walls in radiata pine (Pinus radiata) mild compression wood. Can. J. Bot. 77: 32–40. https://doi.org/10.1139/b98-184.Search in Google Scholar

Singh, A.P., Nilsson, T., and Daniel, G. (1990). Bacterial attack of Pinus sylvestris wood under near-anaerobic conditions. J. Inst. Wood Sci. 11: 237–249.Search in Google Scholar

Singh, A.P., Kim, Y.S., Park, B.D., Chung, G.C., and Wong, A.H.H. (2003). Presence of a distinct S3 layer in mild compression wood tracheids of Pinus radiata. Holzforschung 57: 243–247. https://doi.org/10.1515/hf.2003.03.Search in Google Scholar

Singh, A.P., Kim, Y.S., and Singh, T. (2016). Bacterial degradation of woodKim, Y.S., Funada, R., and Singh, A.P. (Eds.), Secondary xylem biology, Academic Press, London, pp.169–190. https://doi.org/10.1016/b978-0-12-802185-9.00009-7.Search in Google Scholar

Singh, A.P., Kim, Y.S., and Chavan, R.R. (2019). Relationship of wood cell wall ultrastructure to bacterial degradation of wood. IAWA J. 40: 1–26. https://doi.org/10.1163/22941932-40190250.Search in Google Scholar

Timell, T.E. (1986). Compression wood in gymnosperms, Vol. 1. Springer-Verlag, Berlin.10.1007/978-3-642-61616-7Search in Google Scholar

Verhertbruggen, Y., Marcus, S.E., Haeger, A., Ordaz-Ortiz, J.J., and Knox, J.P. (2009). An extended set of monoclonal antibodies to pectic homogalacturonan. Carbohydr. Res. 344: 1858–1862. https://doi.org/10.1016/j.carres.2008.11.010.Search in Google Scholar PubMed

Yeh, T.F., Goldfarb, B., Chang, H.M., Peszlen, L., Braun, J.L., and Kadla, J.F. (2005). Comparison of morphological and chemical properties between juvenile wood and compression wood of loblolly pine. Holzforschung 59: 669–674. https://doi.org/10.1515/hf.2005.107.Search in Google Scholar

Yeh, T.F., Braun, J.L., Goldfarb, B., Chang, H.M., and Kadla, J.F. (2006). Morphological and chemical variations between juvenile wood, mature wood and compression wood of loblolly pine (Pinus taeda L.). Holzforschung 60: 1–8. https://doi.org/10.1515/hf.2006.001.Search in Google Scholar

Yumoto, M., Ishida, S., and Fukazawa, K. (1983). Studies on the formation and structure of the compression wood cells induced by artificial inclination in young trees of Picea glauca: IV. Gradation of the severity of compression wood tracheids. Res. Bull. Coll. Exp. For. Hokkaido Univ. 40: 409–454.Search in Google Scholar

Received: 2022-01-10
Accepted: 2022-04-05
Published Online: 2022-04-26
Published in Print: 2022-07-26

© 2022 Walter de Gruyter GmbH, Berlin/Boston

Downloaded on 20.3.2023 from https://www.degruyter.com/document/doi/10.1515/hf-2022-0005/html
Scroll Up Arrow