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Downloaded October 2014) bioRxiv preprint doi: https://doi.org/10.1101/387308; this version posted August 8, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. Bacterial and fungal contributions to delignification and lignocellulose degradation in forest soils with metagenomic and quantitative stable isotope probing Roland C. Wilhelm, Rahul Singh, Lindsay D. Eltis and William W. Mohn* Department of Microbiology & Immunology, Life Sciences Institute, University of British Columbia, Vancouver, BC, V6T 1Z3, Canada. *Corresponding Author: William Mohn Current address: Department of Microbiology & Immunology, Life Sciences Institute, 2350 Health Sciences Mall, University of British Columbia, Vancouver, BC V6T 1Z3 Tel: +1 604-822-4285 Fax: +1 604-822-6041 Email: [email protected] bioRxiv preprint doi: https://doi.org/10.1101/387308; this version posted August 8, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. Abstract 1 Delignification, or lignin-modification, facilitates the decomposition of lignocellulose in woody 2 plant biomass. The extant diversity of lignin-degrading bacteria and fungi is underestimated by 3 culture-dependent methods, limiting our understanding of the functional and ecological traits of 4 decomposers populations. Here, we describe the use of stable isotope probing (SIP) coupled with 5 amplicon and shotgun metagenomics to identify and characterize the functional attributes of 6 lignin-, cellulose- and hemicellulose-degrading fungi and bacteria in coniferous forest soils from 7 across North America. We tested the extent to which catabolic genes partitioned among different 8 decomposer taxa; the relative roles of bacteria and fungi, and whether taxa or catabolic genes 9 correlated with variation in lignocellulolytic activity, measured as the total assimilation of 13C- 10 label into DNA and phospholipid fatty acids. We found high overall bacterial degradation of our 11 model lignin substrate, particularly by gram-negative bacteria (Comamonadaceae and 12 Caulobacteraceae), while fungi were more prominent in cellulose-degradation. Very few taxa 13 incorporated 13C-label from more than one lignocellulosic polymer, suggesting specialization 14 among decomposers. Collectively, members of Caulobacteraceae could degrade all three 15 lignocellulosic polymers, providing new evidence for their importance in lignocellulose 16 degradation. Variation in lignin-degrading activity was better explained by microbial community 17 properties, such as catabolic gene content and community structure, than cellulose-degrading 18 activity. SIP significantly improved shotgun metagenome assembly resulting in the recovery of 19 several high-quality draft metagenome-assembled genomes and over 7,500 contigs containing 20 unique clusters of carbohydrate-active genes. These results improve understanding of which 21 organisms, conditions and corresponding functional genes contribute to lignocellulose 22 decomposition. 23 Keywords: forest soil, decomposition, stable isotope probing, lignin, cellulose, hemicellulose, 24 metagenomics, PLFA, carbon cycling. 25 Running Title: Lignocellulose Degraders in Forest Soils bioRxiv preprint doi: https://doi.org/10.1101/387308; this version posted August 8, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. Introduction 26 The incomplete decomposition of woody biomass in coniferous forests is an important 27 global carbon sink, with approximately one third of a gigaton of carbon accruing on an annual 28 basis (Myneni et al., 2001). Lignocellulose decomposition is influenced by the structure and 29 function of microbial communities (Strickland et al., 2009; Cleveland et al., 2014) and terrestrial 30 carbon cycling models increasingly parameterize these properties (Allison et al., 2012; Wieder et 31 al., 2015). However, efforts are constrained by our rudimentary knowledge of the composition 32 and ecology of decomposer populations, stemming from limitations of culture-dependent 33 methods and the complexity of soil communities. The best characterized decomposers inhabit 34 forest soil litter, where conditions favour rapid lignocellulose degradation (Melilo et al., 1989; 35 Cortrufo et al., 2015), yet the decay of lignin-rich plant polymers in soil occurs in a continuum 36 governed by conditions and substrate accessibility, resulting in diversified niches for 37 decomposers (von Lützow et al., 2006; Lehmann and Kleber, 2015; Klotzbücher et al., 2015). To 38 resolve the catabolic and ecological traits of decomposers, we must utilize culture-independent 39 methods, like stable isotope probing (SIP), that better reflect in situ conditions. 40 The nature of microbial lignin-degradation is poorly described beyond the canonical 41 breakdown of lignin in woody biomass by specialized, aerobic, litter-inhabiting wood-rot fungi. 42 Yet, these fungi are largely absent in deeper mineral soil where conditions favour decomposition 43 by bacteria (Ekschmitt et al., 2008), who represent the most likely lignin-degraders when oxygen 44 is limited (Benner et al., 1984; DeAngelisa et al., 2011; Hall et al., 2015). Several soil bacteria 45 can degrade model lignin compounds in pure culture, suggesting a role for them in the 46 catabolism of low-molecular weight, partially-degraded forms of lignin (Crawford, 1978; Masai 47 et al., 2007; DeAngelisb et al., 2011; Brown et al., 2012; Taylor et al., 2012; Davis et al., 2013; bioRxiv preprint doi: https://doi.org/10.1101/387308; this version posted August 8, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 48 Rashid et al., 2015). Knowledge of bacterial lignin-degradation in environmental contexts is 49 limited, with all studies of soil degraders originating from tropical forests, which describe active 50 populations of predominantly Alpha- and Gammaproteobacteria (DeAngelisa et al., 2011; Pold et 51 al., 2015). The existing evidence for bacterial lignin-degradation demonstrates the need to 52 characterize both bacterial and fungal populations and contrast their roles in different soil 53 environments to better understand the in situ processes that govern the decomposition of 54 lignocellulose. 55 Delignification rapidly increases the rate of lignocellulose decomposition and may have 56 evolved primarily as a means of accessing more readily degradable plant carbohydrates, 57 exemplified by the strategies of white- and brown-rot Agaricomycota (Eastwood et al., 2011; 58 Ding et al., 2012; Zeng et al., 2014). The capability to co-degrade lignin and other 59 lignocellulosic polymers has not been thoroughly explored in bacteria. There is some evidence 60 for the co-metabolism of lignocellulosic polymers by various Streptomyces spp. (Větrovský et 61 al., 2014), while a comparative genomics study revealed that cellulose-degrading bacteria also 62 possess higher numbers of hemicellulases (Medie et al., 2012). The extent to which catabolic 63 traits are conserved within specific taxa versus communities will influence models of microbial 64 decomposition. In the simplest case, the abundance of highly adapted, multi-substrate degrading 65 taxa may predict rates of decomposition, which is supported by a small number of studies 66 (Strickland et al., 2009; Wilhelma et al., 2017). However, forces of genomic streamlining in 67 bacteria lead to functional diversification among closely related species, particularly in extra- 68 cellular processes that produce common goods (Morris et al., 2012), evident in the species-level 69 conservation of bacterial endoglucanases (Berlemont and Martiny, 2013). A multi-substrate SIP 70 experiment provides the means to identify whether forest soil decomposers can assimilate 13C bioRxiv preprint doi: https://doi.org/10.1101/387308; this version posted August 8, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 71 from various lignocellulosic polymers and, with shotgun metagenomic sequencing, determine 72 whether their genomes encode the necessary suite of catabolic genes. 73 To address the above knowledge gaps, we utilized SIP microcosm-based experiments to 74 investigate the composition and degradative potential of hemicellulose-, cellulose- and lignin- 75 degrading populations from organic and mineral layer soils in coniferous forests across North 76 America. The identity of degraders and their genomic content were assessed using amplicon and 77 shotgun sequencing of DNA enriched in 13C from labeled substrates. Lignocellulolytic activity 78 was quantified according to the amount of 13C assimilated into total DNA and phospholipid fatty 79 acids (PLFA). The in situ abundances of lignocellulolytic populations were determined
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