The feather degradation mechanisms of a new Streptomyces sp. isolate SCUT-3

Communications Biology - Tập 3 Số 1
Zhiwei Li1, Shuang Liang1, Ke Ye2, Jun‐Jin Deng1, Ming-Shu Zhang1, De‐Lin Lu1, Jiansheng Zhang3, Xiao‐Chun Luo1
1School of Biology and Biological Engineering, South China University of Technology, Guangzhou, Guangdong, P. R. China
2Yingdong College of Life Sciences, Shaoguan University, Shaoguan, Guangdong, P. R. China
3Zhanjiang Ocean Sciences and Technologies Research Co. LTD, Zhanjiang, Guangdong, P. R. China

Tóm tắt

AbstractFeather waste is the highest protein-containing resource in nature and is poorly reused. Bioconversion is widely accepted as a low-cost and environmentally benign process, but limited by the availability of safe and highly efficient feather degrading bacteria (FDB) for its industrial-scale fermentation. Excessive focuses on keratinase and limited knowledge of other factors have hindered complete understanding of the mechanisms employed by FDB to utilize feathers and feather cycling in the biosphere. Streptomyces sp. SCUT-3 can efficiently degrade feather to products with high amino acid content, useful as a nutrition source for animals, plants and microorganisms. Using multiple omics and other techniques, we reveal how SCUT-3 turns on its feather utilization machinery, including its colonization, reducing agent and protease secretion, peptide/amino acid importation and metabolism, oxygen consumption and iron uptake, spore formation and resuscitation, and so on. This study would shed light on the feather utilization mechanisms of FDBs.

Từ khóa


Tài liệu tham khảo

Callegaro, K., Welter, N. & Daroit, D. J. Feathers as bioresource: microbial conversion into bioactive protein hydrolysates. Process Biochem. 75, 1–9 (2018).

Kowalczyk, P. et al. Feather-degrading bacteria: their biochemical and genetic characteristics. Arab. J. Sci. Eng. 43, 33–41 (2018).

Lucas, F. S., Broennimann, O., Febbraro, I. & Heeb, P. High diversity among feather-degrading bacteria from a dry meadow soil. Microb. Ecol. 45, 282–290 (2003).

Huang, Y. et al. Production of feather oligopeptides by a newly isolated bacterium Pseudomonas otitis H11. Poult. Sci. (2019). [Epub ahead of print], https://doi.org/10.3382/ps/pez030.

Yang, L. et al. Construction of a rapid feather-degrading bacterium by overexpression of a highly efficient alkaline keratinase in its parent strain Bacillus amyloliquefaciens K11. J. Agric. Food Chem. 64, 78–84 (2016).

Bockle, B. & Muller, R. Reduction of disulfide bonds by Streptomyces pactum during growth on chicken feathers. Appl. Environ. Microbiol. 63, 790–792 (1997).

Grumbt, M. et al. Keratin degradation by dermatophytes relies on cysteine dioxygenase and a sulfite efflux pump. J. Invest. Dermatol. 133, 1550–1555 (2013).

Sharma, R. & Gupta, R. Coupled action of gamma-glutamyl transpeptidase-glutathione and keratinase effectively degrades feather keratin and surrogate prion protein, Sup 35NM. Bioresour. Technol. 120, 314–317 (2012).

Fleck, A. & Munro, H. N. The determination of organic nitrogen in biological materials: a review. Clin. Chim. Acta 11, 2–12 (1965).

Dominy, J. E. Jr., Simmons, C. R., Karplus, P. A., Gehring, A. M. & Stipanuk, M. H. Identification and characterization of bacterial cysteine dioxygenases: a new route of cysteine degradation for eubacteria. J. Bacteriol. 188, 5561–5569 (2006).

Inoue, H. et al. Molecular characterization of the mde operon involved in L-methionine catabolism of Pseudomonas putida. J. Bacteriol. 179, 3956–3962 (1997).

Jothivasan, V. K. & Hamilton, C. J. Mycothiol: synthesis, biosynthesis and biological functions of the major low molecular weight thiol in actinomycetes. Nat. Prod. Rep. 25, 1091–1117 (2008).

Reyes, A. M. et al. Chemistry and redox biology of mycothiol. Antioxid. Redox Signal. 28, 487–504 (2018).

Garai, P., Chandra, K. & Chakravortty, D. Bacterial peptide transporters: messengers of nutrition to virulence. Virulence 8, 297–309 (2017).

Cao, J., Woodhall, M. R., Alvarez, J., Cartron, M. L. & Andrews, S. C. EfeUOB (YcdNOB) is a tripartite, acid-induced and CpxAR-regulated, low-pH Fe2+ transporter that is cryptic in Escherichia coli K-12 but functional in E. coli O157:H7. Mol. Microbiol. 65, 857–875 (2007).

Furrer, J. L., Sanders, D. N., Hook-Barnard, I. G. & McIntosh, M. A. Export of the siderophore enterobactin in Escherichia coli: involvement of a 43 kDa membrane exporter. Mol. Microbiol 44, 1225–1234 (2002).

Kobylarz, M. J. et al. Deciphering the substrate specificity of sbna, the enzyme catalyzing the first step in staphyloferrin b biosynthesis. Biochemistry 55, 927–939 (2016).

Ollinger, J., Song, K. B., Antelmann, H., Hecker, M. & Helmann, J. D. Role of the Fur regulon in iron transport in Bacillus subtilis. J. Bacteriol. 188, 3664–3673 (2006).

Pi, H. & Helmann, J. D. Sequential induction of Fur-regulated genes in response to iron limitation in Bacillus subtilis. Proc. Natl Acad. Sci. U. S. A 114, 12785–12790 (2017).

Pi, H. & Helmann, J.D. Genome-Wide Characterization of the Fur regulatory network reveals a link between catechol degradation and bacillibactin metabolism in Bacillus subtilis. mBio 9, e01451 (2018).

Unden, G. & Bongaerts, J. Alternative respiratory pathways of Escherichia coli: energetics and transcriptional regulation in response to electron acceptors. Biochim. Biophys. Acta—Bioenerg. 1320, 217–234 (1997).

Roberts, D. M., Liao, R. P., Wisedchaisri, G., Hol, W. G. & Sherman, D. R. Two sensor kinases contribute to the hypoxic response of Mycobacterium tuberculosis. J. Biol. Chem. 279, 23082–23087 (2004).

Barriuso-Iglesias, M., Barreiro, C., Sola-Landa, A. & Martín, J. F. Transcriptional control of the F0F1-ATP synthase operon of Corynebacterium glutamicum: SigmaH factor binds to its promoter and regulates its expression at different pH values. Microb. Biotechnol. 6, 178–188 (2013).

Sawers, R.G., Falke, D. & Fischer, M. in Advances in Microbial Physiology Vol. 68. (ed. Poole, R. K.) 1–40 (Academic Press, 2016).

Raffaelli, N. et al. The Escherichia coli NadR regulator is endowed with nicotinamide mononucleotide adenylyltransferase activity. J. Bacteriol. 181, 5509–5511 (1999).

Dresen, C. et al. A flavin-dependent monooxygenase from Mycobacterium tuberculosis involved in cholesterol catabolism. J. Biol. Chem. 285, 22264–22275 (2010).

Umeyama, T., Lee, P. C., Ueda, K. & Horinouchi, S. An AfsK/AfsR system involved in the response of aerial mycelium formation to glucose in Streptomyces griseus. Microbiology 145(Pt 9), 2281–2292 (1999).

Flardh, K. & Buttner, M. J. Streptomyces morphogenetics: dissecting differentiation in a filamentous bacterium. Nat. Rev. Microbiol. 7, 36–49 (2009).

Garg, S. K., Suhail Alam, M., Soni, V., Radha Kishan, K. V. & Agrawal, P. Characterization of Mycobacterium tuberculosis WhiB1/Rv3219 as a protein disulfide reductase. Protein Expr. Purif. 52, 422–432 (2007).

Sexton, D. L. et al. Resuscitation-promoting factors are cell wall-lytic enzymes with important roles in the germination and growth of Streptomyces coelicolor. J. Bacteriol. 197, 848 (2015).

Dutta, T. & Deutscher, M. P. Mode of action of RNase BN/RNase Z on tRNA precursors: RNase BN does not remove the CCA sequence from tRNA. J. Biol. Chem. 285, 22874–22881 (2010).

Tanaka, N. & Shuman, S. RtcB is the RNA ligase component of an Escherichia coli RNA repair operon. J. Biol. Chem. 286, 7727–7731 (2011).

Kumar, S., Das, M., Hadad, C. M. & Musier-Forsyth, K. Aminoacyl-tRNA substrate and enzyme backbone atoms contribute to translational quality control by YbaK. J. Phys. Chem. B. 117, 4521–4527 (2013).

Jain, C. The E. coli RhlE RNA helicase regulates the function of related RNA helicases during ribosome assembly. RNA (New York, NY) 14, 381–389 (2008).

Coatham, M. L., Brandon, H. E., Fischer, J. J., Schümmer, T. & Wieden, H.-J. The conserved GTPase HflX is a ribosome splitting factor that binds to the E-site of the bacterial ribosome. Nucleic Acids Res. 44, 1952–1961 (2016).

Chadani, Y., Ono, K., Kutsukake, K. & Abo, T. Escherichia coli YaeJ protein mediates a novel ribosome-rescue pathway distinct from SsrA- and ArfA-mediated pathways. Mol. Microbiol 80, 772–785 (2011).

Pannekoek, Y. et al. The N5-glutamine S-adenosyl-L-methionine-dependent methyltransferase PrmC/HemK in Chlamydia trachomatis methylates class 1 release factors. J. Bacteriol. 187, 507–511 (2005).

de Oliveira, C. T., Pellenz, L., Pereira, J. Q., Brandelli, A. & Daroit, D. J. Screening of bacteria for protease production and feather degradation. Waste Biomass. Valoriz. 7, 447–453 (2016).

Cedrola, S. M. L. et al. Keratinases and sulfide from Bacillus subtilis SLC to recycle feather waste. J. Microbiol. Biotechnol. 28, 1259–1269 (2012).

Gu, Z. et al. The feather-degrading bacterial community in two soils as revealed by a specific primer targeting serine-type keratinolytic proteases. World J. Microbiol. Biotechnol. 32, 165 (2016).

Zeng, Y. H., Kuo, Y. W. & Chen, H. T. Higher yield of cherry tomato grown in culture medium with microbially inoculated feather compost without fertilizer application. J. Plant Nutr. Soil Sci. 181, 528–536 (2018).

Wang, L. et al. Production and characterization of keratinolytic proteases by a chicken feather-degrading Thermophilic strain, Thermoactinomyces sp. YT06. J. Microbiol. Biotechnol. 27, 2190–2198 (2017).

Jain, P. C. & Agrawal, S. C. A note on the keratin decomposing capability of some fungi. Trans. Mycol. Soc. Jpn. 21, 513–517 (1980).

Fang, Z. et al. Cloning, heterologous expression and characterization of two keratinases from Stenotrophomonas maltophilia BBE11-1. Process Biochem. 49, 647–654 (2014).

Moore, S. & Stein, W. H. A modified ninhydrin reagent for the photometric determination of amino acids and related compounds. J. Biol. Chem. 211, 907–913 (1954).

Ellman, G. L. Tissue sulfhydryl groups. Arch. Biochem Biophys. 82, 70–77 (1959).

Ramnani, P., Singh, R. & Gupta, R. Keratinolytic potential of Bacillus licheniformis RG1: structural and biochemical mechanism of feather degradation. Can. J. Microbiol. 51, 191–196 (2005).

Kumar, S., Stecher, G. & Tamura, K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33, 1870–1874 (2016).

Yoon, S. H., Ha, S. M., Lim, J., Kwon, S. & Chun, J. A large-scale evaluation of algorithms to calculate average nucleotide identity. Antonie Van. Leeuwenhoek 110, 1281–1286 (2017).

Yu, G., Wang, L. G., Han, Y. & He, Q. Y. clusterProfiler: an R package for comparing biological themes among gene clusters. OMICS 16, 284–287 (2012).

Thorvaldsdottir, H., Robinson, J. T. & Mesirov, J. P. Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief. Bioinform. 14, 178–192 (2013).

Bierman, M. et al. Plasmid cloning vectors for the conjugal transfer of DNA from Escherichia coli to Streptomyces spp. Gene 116, 43–49 (1992).