Soil bacterial depth distribution controlled by soil orders and soil forms

Peipei Xue, Alex B. McBratney, Budiman Minasny, Tony O'Donnell, Vanessa Pino, Mario Fajardo, Wartini Ng, Neil Wilson, Rosalind Deaker

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Soil Ecology Letters ›› 2022, Vol. 4 ›› Issue (1) : 57-68. DOI: 10.1007/s42832-020-0072-0
RESEARCH ARTICLE
RESEARCH ARTICLE

Soil bacterial depth distribution controlled by soil orders and soil forms

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Highlights

• Topsoil diversity was greater in phenosoils than genosoils, but the trend was reversed in subsoils.

• Bacterial community in topsoils was influenced by both soil orders and soil forms, however, in subsoils it was more impacted by soil orders.

• Cropping increased the similarity of bacteria structures among different soil orders.

Abstract

Human disturbances to soils can lead to dramatic changes in soil physical, chemical, and biological properties. The influence of agricultural activities on the bacterial community over different orders of soil and at depth is still not well understood. We used the concept of genoform and phenoform to investigate the vertical (down to 1 m depth) soil bacterial community structure in paired genosoils (undisturbed forests) and phenosoils (cultivated vineyards) in different soil orders. The study was conducted in the Hunter Valley area, New South Wales, Australia, where samples were collected from 3 different soil orders (Calcarosol, Chromosol, and Kurosol), and each soil order consists of a pair of genosoil and phenosoil. The bacterial community structure was analyzed using high-throughput sequencing of 16S rRNA. Results showed that bacterial-diversity decreased with depth in phenosoils, however, the trend is less obvious in genoform profiles. Topsoil diversity was greater in phenosoils than genosoils, but the trend was reversed in subsoils. Thus, cropping not only affected topsoil bacteria community but also decreased its diversity in the subsoil. Bacterial community in topsoils was influenced by both soil orders and soil forms, however, in subsoils it was more impacted by soil orders. Constrained Analysis of Principal Coordinates revealed that cropping increased the similarity of bacterial structures of different soil orders. This study highlighted the strong influence of agricultural activities on soil microbial distribution with depth, which is controlled by soil orde

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Keywords

Bacterial distribution / Soil depth / Soil forms/land use / Genosoil and phenosoil / Soil type/soil order

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Peipei Xue, Alex B. McBratney, Budiman Minasny, Tony O'Donnell, Vanessa Pino, Mario Fajardo, Wartini Ng, Neil Wilson, Rosalind Deaker. Soil bacterial depth distribution controlled by soil orders and soil forms. Soil Ecology Letters, 2022, 4(1): 57‒68 https://doi.org/10.1007/s42832-020-0072-0

References

[1]
Aguirre-von-Wobeser, E., Rocha-Estrada, J., Shapiro, L.R., de la Torre, M., 2018. Enrichment of Verrucomicrobia, Actinobacteria and Burkholderiales drives selection of bacterial community from soil by maize roots in a traditional milpa agroecosystem. PLoS One 13, e0208852
CrossRef Google scholar
[2]
Anandan, R., Dharumadurai, D., Manogaran, G.P., 2016. An Introduction to Actinobacteria. In: Dhanasekaran, D., Jiang, Y., eds. Actinobacteria-Basics and Biotechnological Applications. Intechopen.
[3]
Anderson, M.J., Willis, T.J., 2003. Canonical analysis of principal coordinates: a useful method of constrained ordination for ecology. Ecology 84, 511–525
CrossRef Google scholar
[4]
Bardgett, R.D., Van Der Putten, W.H., 2014. Belowground biodiversity and ecosystem functioning. Nature 515, 505–511
CrossRef Google scholar
[5]
Barns, S.M., Takala, S.L., Kuske, C.R., 1999. Wide distribution and diversity of members of the bacterial kingdom Acidobacterium in the environment. Applied and Environmental Microbiology 65, 1731–1737
CrossRef Google scholar
[6]
Bolyen, E., Rideout, J.R., Dillon, M.R., Bokulich, N.A., Abnet, C.C., Al-Ghalith, G.A., Alexander, H., Alm, E.J., Arumugam, M., Asnicar, F., Bai, Y., Bisanz, J.E., Bittinger, K., Brejnrod, A., Brislawn, C.J., Brown, C.T., Callahan, B.J., Caraballo-Rodríguez, A.M., Chase, J., Cope, E.K., Da Silva, R., Diener, C., Dorrestein, P.C., Douglas, G.M., Durall, D.M., Duvallet, C., Edwardson, C.F., Ernst, M., Estaki, M., Fouquier, J., Gauglitz, J.M., Gibbons, S.M., Gibson, D.L., Gonzalez, A., Gorlick, K., Guo, J., Hillmann, B., Holmes, S., Holste, H., Huttenhower, C., Huttley, G.A., Janssen, S., Jarmusch, A.K., Jiang, L., Kaehler, B.D., Kang, K.B., Keefe, C.R., Keim, P., Kelley, S.T., Knights, D., Koester, I., Kosciolek, T., Kreps, J., Langille, M.G.I., Lee, J., Ley, R., Liu, Y.X., Loftfield, E., Lozupone, C., Maher, M., Marotz, C., Martin, B.D., McDonald, D., McIver, L.J., Melnik, A.V., Metcalf, J.L., Morgan, S.C., Morton, J.T., Naimey, A.T., Navas-Molina, J.A., Nothias, L.F., Orchanian, S.B., Pearson, T., Peoples, S.L., Petras, D., Preuss, M.L., Pruesse, E., Rasmussen, L.B., Rivers, A., Robeson, M.S. II, Rosenthal, P., Segata, N., Shaffer, M., Shiffer, A., Sinha, R., Song, S.J., Spear, J.R., Swafford, A.D., Thompson, L.R., Torres, P.J., Trinh, P., Tripathi, A., Turnbaugh, P.J., Ul-Hasan, S., van Der Hooft, J.J.J., Vargas, F., Vázquez-Baeza, Y., Vogtmann, E., Von Hippel, M., Walters, W., Wan, Y., Wang, M., Warren, J., Weber, K.C., Williamson, C.H.D., Willis, A.D., Xu, Z.Z., Zaneveld, J.R., Zhang, Y., Zhu, Q., Knight, R., Caporaso, J.G., 2019. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nature Biotechnology 37, 852–857
CrossRef Google scholar
[7]
Brandt, A.J., de Kroon, H., Reynolds, H.L., Burns, J.H., 2013. Soil heterogeneity generated by plant–soil feedbacks has implications for species recruitment and coexistence. Journal of Ecology 101, 277–286
CrossRef Google scholar
[8]
Brewer, T.E., Aronson, E.L., Arogyaswamy, K., Billings, S.A., Botthoff, J.K., Campbell, A.N., Dove, N.C., Fairbanks, D., Gallery, R.E., Hart, S.C., Kaye, J., King, G., Logan, G., Lohse, K.A., Maltz, M.R., Mayorga, E., O’Neill, C., Owens, S.M., Packman, A., Pett-Ridge, J., Plante, A.F., Richter, D.D., Silver, W.L., Yang, W.H., Fierer, N., 2019. Ecological and genomic attributes of novel bacterial taxa that thrive in subsurface soil horizons. mBio 10, e01318–e01319
CrossRef Google scholar
[9]
Bureau of Meteorology, 2019. Climate statistics for Australian locations. Australian Government.
[10]
Callahan, B., 2018. Silva taxonomic training data formatted for DADA2 (Silva version 132).
[11]
Callahan, B., Sankaran, K., Fukuyama, J.A., McMurdie, P.J., Holmes, S.P., 2016. Bioconductor workflow for microbiome data analysis: from raw reads to community analyses. F1000 Research 5:1492.
[12]
Callahan, B., Sankaran, K., Fukuyama, J.A., McMurdie, P.J., Holmes, S.P., 2019. DADA2 Pipeline Tutorial (1.12).
[13]
Conradie, T., Jacobs, K., 2020. Seasonal and agricultural response of Acidobacteria present in two fynbos rhizosphere soils. Diversity (Basel) 12, 277
CrossRef Google scholar
[14]
Crowther, T.W., Van den Hoogen, J., Wan, J., Mayes, M.A., Keiser, A., Mo, L., Averill, C., Maynard, D.S., 2019. The global soil community and its influence on biogeochemistry. Science 365, eaav0550.
[15]
Delgado-Baquerizo, M., Maestre, F.T., Reich, P.B., Jeffries, T.C., Gaitan, J.J., Encinar, D., Berdugo, M., Campbell, C.D., Singh, B.K., 2016. Microbial diversity drives multifunctionality in terrestrial ecosystems. Nature Communications 7, 10541
CrossRef Google scholar
[16]
Dixon, P., 2003. VEGAN, a package of R functions for community ecology. Journal of Vegetation Science 14, 927–930
CrossRef Google scholar
[17]
Droogers, P., Bouma, J., 1997. Soil survey input in exploratory modeling of sustainable soil management practices. Soil Science Society of America Journal 61, 1704–1710
CrossRef Google scholar
[18]
Eilers, K.G., Debenport, S., Anderson, S., Fierer, N., 2012. Digging deeper to find unique microbial communities: The strong effect of depth on the structure of bacterial and archaeal communities in soil. Soil Biology & Biochemistry 50, 58–65
CrossRef Google scholar
[19]
Fierer, N., 2017. Embracing the unknown: disentangling the complexities of the soil microbiome. Nature Reviews. Microbiology 15, 579–590
CrossRef Google scholar
[20]
Fierer, N., Schimel, J.P., Holden, P.A., 2003. Variations in microbial community composition through two soil depth profiles. Soil Biology & Biochemistry 35, 167–176
CrossRef Google scholar
[21]
Garcia-Pichel, F., Johnson, S.L., Youngkin, D., Belnap, J., 2003. Small-scale vertical distribution of bacterial biomass and diversity in biological soil crusts from arid lands in the Colorado Plateau. Microbial Ecology 46, 312–321
CrossRef Google scholar
[22]
Geisen, S., Wall, D.H., van der Putten, W.H., 2019. Challenges and opportunities for soil biodiversity in the Anthropocene. Current Biology 29, R1036–R1044
CrossRef Google scholar
[23]
Hartmann, M., Lee, S., Hallam, S.J., Mohn, W.W., 2009. Bacterial, archaeal and eukaryal community structures throughout soil horizons of harvested and naturally disturbed forest stands. Environmental Microbiology 11, 3045–3062
CrossRef Google scholar
[24]
Hendgen, M., Hoppe, B., Döring, J., Friedel, M., Kauer, R., Frisch, M., Dahl, A., Kellner, H., 2018. Effects of different management regimes on microbial biodiversity in vineyard soils. Scientific Reports 8, 9393
CrossRef Google scholar
[25]
Hsiao, C.J., Sassenrath, G.F., Zeglin, L.H., Hettiarachchi, G.M., Rice, C.W., 2018. Vertical changes of soil microbial properties in claypan soils. Soil Biology & Biochemistry 121, 154–164
CrossRef Google scholar
[26]
Hu, Y., Xiang, D., Veresoglou, S.D., Chen, F., Chen, Y., Hao, Z., Zhang, X., Chen, B., 2014. Soil organic carbon and soil structure are driving microbial abundance and community composition across the arid and semi-arid grasslands in northern China. Soil Biology & Biochemistry 77, 51–57
CrossRef Google scholar
[27]
Huang, J., McBratney, A.B., Malone, B.P., Field, D.J., 2018. Mapping the transition from pre-European settlement to contemporary soil conditions in the Lower Hunter Valley, Australia. Geoderma 329, 27–42
CrossRef Google scholar
[28]
Jiang, X., Wright, A.L., Wang, J., Li, Z., 2011. Long-term tillage effects on the distribution patterns of microbial biomass and activities within soil aggregates. Catena 87, 276–280
CrossRef Google scholar
[29]
Jiao, S., Chen, W., Wang, J., Du, N., Li, Q., Wei, G., 2018. Soil microbiomes with distinct assemblies through vertical soil profiles drive the cycling of multiple nutrients in reforested ecosystems. Microbiome 6, 1–13
CrossRef Google scholar
[30]
Johan, H., Corrie, S., 2015. Effects of conservation agriculture and fertilization on soil microbial diversity and activity. Environments 2, 358–384
CrossRef Google scholar
[31]
Jones, D.L., Magthab, E.A., Gleeson, D.B., Hill, P.W., Sánchez-Rodríguez, A.R., Roberts, P., Ge, T., Murphy, D.V., 2018. Microbial competition for nitrogen and carbon is as intense in the subsoil as in the topsoil. Soil Biology & Biochemistry 117, 72–82
CrossRef Google scholar
[32]
Lagerlöf, J., Adolfsson, L., Börjesson, G., Ehlers, K., Vinyoles, G.P., Sundh, I., 2014. Land-use intensification and agroforestry in the Kenyan highland: Impacts on soil microbial community composition and functional capacity. Applied Soil Ecology 82, 93–99
CrossRef Google scholar
[33]
Li, C., Yan, K., Tang, L., Jia, Z., Li, Y., 2014. Change in deep soil microbial communities due to long-term fertilization. Soil Biology & Biochemistry 75, 264–272
CrossRef Google scholar
[34]
Lienhard, P., Terrat, S., Prévost-Bouré, N.C., Nowak, V., Régnier, T., Sayphoummie, S., Panyasiri, K., Tivet, F., Mathieu, O., Levêque, J., Maron, P.A., Ranjard, L., 2014. Pyrosequencing evidences the impact of cropping on soil bacterial and fungal diversity in Laos tropical grassland. Agronomy for Sustainable Development 34, 525–533
CrossRef Google scholar
[35]
Lozupone, C., Lladser, M.E., Knights, D., Stombaugh, J., Knight, R., 2011. UniFrac: an effective distance metric for microbial community comparison. ISME Journal 5, 169–172
CrossRef Google scholar
[36]
Luo, P., Han, X., Wang, Y., Han, M., Shi, H., Liu, N., Bai, H., 2015. Influence of long-term fertilization on soil microbial biomass, dehydrogenase activity, and bacterial and fungal community structure in a brown soil of northeast China. Annals of Microbiology 65, 533–542
CrossRef Google scholar
[37]
Millard, P., Singh, B., 2010. Does grassland vegetation drive soil microbial diversity? Nutrient Cycling in Agroecosystems 88, 147–158
CrossRef Google scholar
[38]
Nazaries, L., Karunaratne, S.B., Delgado-Baquerizo, M., Campbell, C.D., Singh, B.K., 2018. Environmental drivers of the geographical distribution of methanotrophs: Insights from a national survey. Soil Biology & Biochemistry 127, 264–279
CrossRef Google scholar
[39]
Ng, W., Malone, B.P., Minasny, B., 2017. Rapid assessment of petroleum-contaminated soils with infrared spectroscopy. Geoderma 289, 150–160
CrossRef Google scholar
[40]
Nogueira, M., Ribeiro Vasconcelos, A., Hungria, M., 2016. Shifts in taxonomic and functional microbial diversity with agriculture: How fragile is the Brazilian Cerrado? BMC Microbiology 16, 42
[41]
O’Brien, S.L., Gibbons, S.M., Owens, S.M., Hampton‐Marcell, J., Johnston, E.R., Jastrow, J.D., Gilbert, J.A., MeyerF., Antonopoulos, D.A., 2016. Spatial scale drives patterns in soil bacterial diversity. Environmental Microbiology 18, 2039–2051
CrossRef Google scholar
[42]
Plassart, P., Prévost-Bouré, N.C., Uroz, S., Dequiedt, S., Stone, D., Creamer, R., Griffiths, R.I., Bailey, M.J., Ranjard, L., Lemanceau, P., 2019. Soil parameters, land use, and geographical distance drive soil bacterial communities along a European transect. Scientific Reports 9, 605
CrossRef Google scholar
[43]
Rillig, M.C., Ryo, M., Lehmann, A., Aguilar-Trigueros, C.A., Buchert, S., Wulf, A., Iwasaki, A., Roy, J., Yang, G., 2019. The role of multiple global change factors in driving soil functions and microbial biodiversity. Science 366, 886–890
CrossRef Google scholar
[44]
Rossiter, D.G., Bouma, J., 2018. A new look at soil phenoforms–Definition, identification, mapping. Geoderma 314, 113–121
CrossRef Google scholar
[45]
Scharroba, A., Dibbern, D., Hünninghaus, M., Kramer, S., Moll, J., Butenschoen, O., Bonkowski, M., Buscot, F., Kandeler, E., Koller, R., Krüger, D., Lueders, T., Scheu, S., Ruess, L., 2012. Effects of resource availability and quality on the structure of the micro-food web of an arable soil across depth. Soil Biology & Biochemistry 50, 1–11
CrossRef Google scholar
[46]
Schlatter, D.C., Kahl, K., Carlson, B., Huggins, D.R., Paulitz, T., 2020. Soil acidification modifies soil depth-microbiome relationships in a no-till wheat cropping system. Soil Biology & Biochemistry 149, 107939
CrossRef Google scholar
[47]
Seuradge, B.J., Oelbermann, M., Neufeld, J.D., 2016. Depth-dependent influence of different land-use systems on bacterial biogeography. FEMS Microbiology Ecology93, fiw239.
[48]
Söderström, B., Hedlund, K., Jackson, L.E., Kätterer, T., Lugato, E., Thomsen, I.K., Bracht Jørgensen, H., 2014. What are the effects of agricultural management on soil organic carbon (SOC) stocks? Environmental Evidence 3, 2
CrossRef Google scholar
[49]
Stone, M., DeForest, J., Plante, A., 2014. Changes in extracellular enzyme activity and microbial community structure with soil depth at the Luquillo Critical Zone Observatory. Soil Biology & Biochemistry 75, 237–247
CrossRef Google scholar
[50]
Suela Silva, M., Naves Sales, A., Teixeira Magalhães-Guedes, K., Ribeiro Dias, D., Schwan, R.F., 2013. Brazilian Cerrado soil Actinobacteria ecology. BioMed Research International 2013, 503805–503805
CrossRef Google scholar
[51]
Sui, X., Zhang, R., Frey, B., Yang, L., Li, M.H., Ni, H., 2019. Land use change effects on diversity of soil bacterial, Acidobacterial and fungal communities in wetlands of the Sanjiang Plain, northeastern China. Scientific Reports 9, 18535
CrossRef Google scholar
[52]
Takahashi, S., Tomita, J., Nishioka, K., Hisada, T., Nishijima, M., 2014. Development of a prokaryotic universal primer for simultaneous analysis of bacteria and archaea using next-generation sequencing. PLoS One 9, e105592
CrossRef Google scholar
[53]
Tardy, V., Spor, A., Mathieu, O., Lévèque, J., Terrat, S., Plassart, P., Regnier, T., Bardgett, R.D., van der Putten, W.H., Roggero, P.P., Seddaiu, G., Bagella, S., Lemanceau, P., Ranjard, L., Maron, P.A., 2015. Shifts in microbial diversity through land use intensity as drivers of carbon mineralization in soil. Soil Biology & Biochemistry 90, 204–213
CrossRef Google scholar
[54]
Thakur, M.P., Phillips, H.R.P., Brose, U., De Vries, F.T., Lavelle, P., Loreau, M., Mathieu, J., Mulder, C., Van der Putten, W.H., Rillig, M.C., Wardle, D.A., Bach, E.M., Bartz, M.L.C., Bennett, J.M., Briones, M.J.I., Brown, G., Decaëns, T., Eisenhauer, N., Ferlian, O., Guerra, C.A., König-Ries, B., Orgiazzi, A., Ramirez, K.S., Russell, D.J., Rutgers, M., Wall, D.H., Cameron, E.K., 2020. Towards an integrative understanding of soil biodiversity. Biological Reviews of the Cambridge Philosophical Society 95, 350–364
CrossRef Google scholar
[55]
Tripathi, B.M., Kim, M., Lai-Hoe, A., Shukor, N.A., Rahim, R.A., Go, R., Adams, J.M., 2013. pH dominates variation in tropical soil archaeal diversity and community structure. FEMS Microbiology Ecology 86, 303–311
CrossRef Google scholar
[56]
Trivedi, C., Reich, P.B., Maestre, F.T., Hu, H.W., Singh, B.K., Delgado-Baquerizo, M., 2019. Plant-driven niche differentiation of ammonia-oxidizing bacteria and archaea in global drylands. ISME Journal 13, 2727–2736
CrossRef Google scholar
[57]
Upton, R.N., Checinska Sielaff, A., Hofmockel, K.S., Xu, X., Polley, H.W., Wilsey, B.J., 2020. Soil depth and grassland origin cooperatively shape microbial community co-occurrence and function. Ecosphere 11, e02973
CrossRef Google scholar
[58]
Uri, Y.L., Tracy, K.T., Robertson, G.P., Thomas, M.S., 2011. Agriculture’s impact on microbial diversity and associated fluxes of carbon dioxide and methane. ISME Journal 5, 1683–1691
CrossRef Google scholar
[59]
Van Der Heijden, M.G., Bardgett, R.D., Van Straalen, N.M., 2008. The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecology Letters 11, 296–310
CrossRef Google scholar
[60]
Van Leeuwen, J., Djukic, I., Bloem, J., Lehtinen, T., Hemerik, L., de Ruiter, P., Lair, G., 2017. Effects of land use on soil microbial biomass, activity and community structure at different soil depths in the Danube floodplain. European Journal of Soil Biology 79, 14–20
CrossRef Google scholar
[61]
Wagg, C., Bender, S.F., Widmer, F., van der Heijden, M.G., 2014. Soil biodiversity and soil community composition determine ecosystem multifunctionality. Proceedings of the National Academy of Sciences of the United States of America 111, 5266–5270
CrossRef Google scholar
[62]
Wang, Y., Li, Y., Ye, X., Chu, Y., Wang, X., 2010. Profile storage of organic/inorganic carbon in soil: From forest to desert. Science of the Total Environment 408, 1925–1931
CrossRef Google scholar
[63]
Wang, Z., Li, T., Li, Y., Zhao, D., Han, J., Liu, Y., Liao, Y., 2020. Relationship between the microbial community and catabolic diversity in response to conservation tillage. Soil & Tillage Research 196, 104431
CrossRef Google scholar
[64]
Wenhui, Z., Zucong, C., Lichu, Y., He, Z., 2007. Effects of the long-term application of inorganic fertilizers on microbial community diversity in rice-planting red soil as studied by using PCR-DGGE. Acta Ecologica Sinica 27, 4011–4018
CrossRef Google scholar
[65]
Wickham, H., 2016. ggplot2: elegant graphics for data analysis. Springer, Berlin.
[66]
Will, C., Thurmer, A., Wollherr, A., Nacke, H., Herold, N., Schrumpf, M., Gutknecht, J., Wubet, T., Buscot, F., Daniel, R., 2010. Horizon-specific bacterial community composition of german grassland soils, as revealed by pyrosequencing-based analysis of 16S rRNA genes. Applied and Environmental Microbiology 76, 6751
CrossRef Google scholar
[67]
Wu, H., Adams, J.M., Shi, Y., Li, Y., Song, X., Zhao, X., Chu, H., Zhang, G.L., 2020. Depth-dependent patterns of bacterial communities and assembly processes in a typical red soil critical zone. Geomicrobiology Journal 37, 201–212
CrossRef Google scholar
[68]
Xia, Q., Rufty, T., Shi, W., 2020. Soil microbial diversity and composition: Links to soil texture and associated properties. Soil Biology & Biochemistry 149, 107953
CrossRef Google scholar
[69]
Xue, P., Carrillo, Y., Pino, V., Minasny, B., McBratney, A.B., 2018. Soil properties drive microbial community structure in a large scale transect in south eastern Australia. Scientific Reports 8, 11725
CrossRef Google scholar
[70]
Young, I.M., Crawford, J.W., 2004. Interactions and self-organization in the soil-microbe complex. Science 304, 1634–1637
CrossRef Google scholar
[71]
Zhalnina, K., Dias, R., Quadros, P., Davis-Richardson, A., Camargo, F., Clark, I., McGrath, S., Hirsch, P., Triplett, E., 2015. Soil pH determines microbial diversity and composition in the park grass experiment. Microbial Ecology 69, 395–406
CrossRef Google scholar

Acknowledgment

This work was supported by the ARC Discovery project DP190103005 Synergising pedodiversity and soil biodiversity to secure soil functionality.

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