Evolution of High Cellulolytic Activity in Symbiotic Streptomyces through Selection of Expanded Gene Content and Coordinated Gene Expression

PLoS Biology

Volumn 14, Issue 6, 2016, Pages

  Book, Adam J ^a   Lewin, Gina R ^a   McDonald, Bradon R ^a   Takasuka, Taichi E ^a   Wendt Pienkowski, Evelyn ^a   Doering, Drew T ^a   Suh, Steven ^a   Raffa, Kenneth F ^a   Fox, Brian G ^a   Currie, Cameron R ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ENZYME; CARBOHYDRATE ACTIVE ENZYME; CELLULOSE; CELLULOSE 1,4 BETA CELLOBIOSIDASE; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; CELLULASE; RNA 16S;

ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BIOMASS; CAZY GENE; CEBR GENE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME DEGRADATION; ENZYME REGULATION; GENE CONTENT; GENE DELETION; GENE EXPRESSION; GENE TARGETING; GENETIC PARAMETERS; GENOME ANALYSIS; HOST; MOLECULAR EVOLUTION; NONHUMAN; PHYLOGENY; PLANT BIOMASS DESTRUCTION; PROTEIN EXPRESSION; PROTEOMICS; SEQUENCE ANALYSIS; SOIL MICROFLORA; STRAIN DIFFERENCE; STREPTOMYCES; SYMBIOSIS; TRANSCRIPTOMICS; CLASSIFICATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC SELECTION; GENETICS; GENOMICS; HYDROLYSIS; METABOLISM; MICROBIOLOGY; PLANT; PROCEDURES; SPECIES DIFFERENCE;

BACTERIAL PROTEINS; BIOMASS; CELLULASE; CELLULOSE; EVOLUTION, MOLECULAR; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENOMICS; HYDROLYSIS; PHYLOGENY; PLANTS; RNA, RIBOSOMAL, 16S; SELECTION, GENETIC; SOIL MICROBIOLOGY; SPECIES SPECIFICITY; STREPTOMYCES; SYMBIOSIS;

EID: 84979076138     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1002475     Document Type: Article

References (82)

1. Schlesinger WH, Andrews JA, Soil respiration and the global carbon cycle. Biogeochemistry. 2000;48(1):7–20.
2. Zhao ZT, Liu HQ, Wang CF, Xu J-R, Comparative analysis of fungal genomes reveals different plant cell wall degrading capacity in fungi. BMC Genomics. 2013;14:274.
3. Berlemont R, Martiny AC, Phylogenetic distribution of potential cellulases in bacteria. Appl Environ Microbiol. 2013;79(5):1545–54.
4. Glass NL, Schmoll M, Cate JH, Coradetti S, Plant cell wall deconstruction by ascomycete fungi. Annu Rev Microbiol. 2013;67:477–98. doi: 10.1146/annurev-micro-092611-15004423808333
5. Lynd LR, Weimer PJ, van Zyl WH, Pretorius IS, Microbial cellulose utilization: Fundamentals and biotechnology. Microbiol Mol Biol Rev. 2002;66(3):506–77. 12209002
6. Matulich KL, Martiny JBH, Microbial composition alters the response of litter decomposition to environmental change. Ecology. 2015;96(1):154–63. 26236900
7. McGuire KL, Treseder KK, Microbial communities and their relevance for ecosystem models: Decomposition as a case study. Soil Biol Biochem. 2010;42(4):529–35.
8. Bouws H, Wattenberg A, Zorn H, Fungal secretomes—nature's toolbox for white biotechnology. Appl Microbiol Biotechnol. 2008;80(3):381–8. doi: 10.1007/s00253-008-1572-518636256
9. Gilbert HJ, Cellulosomes: microbial nanomachines that display plasticity in quaternary structure. Mol Microbiol. 2007;63(6):1568–76. 17367380
10. Schuster A, Schmoll M, Biology and biotechnology of Trichoderma. Appl Microbiol Biotechnol. 2010;87(3):787–99. doi: 10.1007/s00253-010-2632-120461510
11. Takasuka TE, Book AJ, Lewin GR, Currie CR, Fox BG, Aerobic deconstruction of cellulosic biomass by an insect-associated Streptomyces. Sci Rep. 2013;3:1030.
12. Wilson DB, Microbial diversity of cellulose hydrolysis. Curr Opin Microbiol. 2011;14(3):259–63.
13. Floudas D, Binder M, Riley R, Barry K, Blanchette RA, Henrissat B, et al. The Paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science. 2012;336(6089):1715–9. doi: 10.1126/science.122174822745431
14. Kohler A, Kuo A, Nagy LG, Morin E, Barry KW, Buscot F, et al. Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists. Nat Genet. 2015;47(4):410–5. doi: 10.1038/ng.322325706625
15. Chater KF, Biro S, Lee KJ, Palmer T, Schrempf H, The complex extracellular biology of Streptomyces. FEMS Microbiol Rev. 2010;34(2):171–98. doi: 10.1111/j.1574-6976.2009.00206.x20088961
16. Kieser T, Buttner MJ, Chater KF, Hopwood DA. Practical Streptomyces genetics. Colney: John Innes Foundation; 2000.
17. Schremph H, Dworkin M, Biology of Streptomycetes. 3rd. ed. New York: Springer-Verlag; 2007.
18. Aylward FO, Suen G, Biedermann PHW, Adams AS, Scott JJ, Malfatti SA, et al. Convergent bacterial microbiotas in the fungal agricultural systems of insects. Mbio. 2014;5(6):e02077.
19. Janssen PH, Identifying the dominant soil bacterial taxa in libraries of 16S rRNA and 16S rRNA genes. Appl Environ Microbiol. 2006;72(3):1719–28.
20. Adams AS, Jordan MS, Adams SM, Suen G, Goodwin LA, Davenport KW, et al. Cellulose-degrading bacteria associated with the invasive woodwasp Sirex noctilio. ISME J. 2011;5(8):1323–31. doi: 10.1038/ismej.2011.1421368904
21. Schatz A, Bugle E, Waksman SA, Streptomycin, a substance exhibiting antibiotic activity against gram-positive and gram-negative bacteria. Exp Biol Med. 1944;55(1):66–9.
22. Hopwood DA, Streptomyces in nature and medicine: the antibiotic makers. New York: Oxford University Press; 2007.
23. Doroghazi JR, Metcalf WW, Comparative genomics of actinomycetes with a focus on natural product biosynthetic genes. BMC genomics. 2013;14:611. doi: 10.1186/1471-2164-14-61124020438
24. Bontemps C, Toussaint M, Revol PV, Hotel L, Jeanbille M, Uroz S, et al. Taxonomic and functional diversity of Streptomyces in a forest soil. FEMS Microbiol Lett. 2013;342(2):157–67. doi: 10.1111/1574-6968.1212623489323
25. Hanshew AS, McDonald BR, Diaz Diaz C, Djieto-Lordon C, Blatrix R, Currie CR, Characterization of Actinobacteria associated with three ant-plant mutualisms. Microb Ecol. 2015;69(1):192–203. doi: 10.1007/s00248-014-0469-325096989
26. Book AJ, Lewin GR, McDonald BR, Takasuka TE, Doering DT, Adams AS, et al. Cellulolytic Streptomyces strains associated with herbivorous insects share a phylogenetically linked capacity to degrade lignocellulose. Appl Environ Microbiol. 2014;80(15):4692–701.
27. Bibb MJ, Regulation of secondary metabolism in streptomycetes. Curr Opin Microbiol. 2005;8(2):208–15.
28. Hopwood DA, Chater KF, Bibb MJ, Genetics of antibiotic production in Streptomyces coelicolor A3(2), a model streptomycete. Biotechnology. 1995;28:65–102. 8688641
29. Wachinger G, Bronnenmeier K, Staudenbauer WL, Schrempf H, Identification of mycelium-associated cellulase from Streptomyces reticuli. Appl Environ Microbiol. 1989;55(10):2653–7.
30. Saratale GD, Saratale RG, Oh SE, Production and characterization of multiple cellulolytic enzymes by isolated Streptomyces sp. MDS. Biomass Bioenergy. 2012;47:302–15.
31. Whiteley M, Bangera MG, Bumgarner RE, Parsek MR, Teitzel GM, Lory S, et al. Gene expression in Pseudomonas aeruginosa biofilms. Nature. 2001;413(6858):860–4. 11677611
32. de Boer W, Folman LB, Summerbell RC, Boddy L, Living in a fungal world: impact of fungi on soil bacterial niche development. FEMS Microbiol Rev. 2005;29(4):795–811. 16102603
33. Pullan ST, Chandra G, Bibb MJ, Merrick M, Genome-wide analysis of the role of GlnR in Streptomyces venezualae provides new insights into global nitrogen regulation in actinomycetes. BMC genomics. 2011;12:175. doi: 10.1186/1471-2164-12-17521463507
34. Liao CH, Yao L, Xu Y, Liu WB, Zhou Y, Ye BC, Nitrogen regulator GlnR controls uptake and utilization of non-phosphotransferase-system carbon sources in actinomycetes. Proc Natl Acad Sci U S A. 2015;112(51):15630–5. doi: 10.1073/pnas.150846511226644570
35. Himmel ME, Ding SY, Johnson DK, Adney WS, Nimlos MR, Brady JW, et al. Biomass recalcitrance: Engineering plants and enzymes for biofuels production. Science. 2007;315(5813):804–7. 17289988
36. Scott JJ, Oh DC, Yuceer MC, Klepzig KD, Clardy J, Currie CR, Bacterial protection of beetle-fungus mutualism. Science. 2008;322(5898):63. doi: 10.1126/science.116042318832638
37. Schlosser A, Schrempf H, A lipid-anchored binding protein is a component of an ATP-dependent cellobiose/cellotriose-transport system from the cellulose degrader Streptomyces reticuli. Eur J Biochem. 1996;242(2):332–8. 8973652
38. Schlosser A, Jantos J, Hackmann K, Schrempf H, Characterization of the binding protein-dependent cellobiose and cellotriose transport system of the cellulose degrader Streptomyces reticuli. Appl Environ Microbiol. 1999;65(6):2636–43. 10347054
39. Marushima K, Ohnishi Y, Horinouchi S, CebR as a master regulator for cellulose/cellooligosaccharide catabolism affects morphological development in Streptomyces griseus. J Bacteriol. 2009;191(19):5930–40. doi: 10.1128/JB.00703-0919648249
40. Walter S, Schrempf H, The synthesis of the Streptomyces reticuli cellulase (Avicelase) is regulated by both activation and repression mechanisms. Mol Gen Genet. 1996;251(2):186–95. 8668129
41. Anderson I, Abt B, Lykidis A, Klenk HP, Kyrpides N, Ivanova N, Genomics of aerobic cellulose utilization systems in Actinobacteria. PLoS ONE. 2012;7(6):e39331.
42. Spiridonov NA, Wilson DB, Characterization and cloning of CelR, a transcriptional regulator of cellulase genes from Thermomonospora fusca. J Biol Chem. 1999;274(19):13127–32. 10224066
43. Francis IM, Jourdan S, Fanara S, Loria R, Rigali S, The cellobiose sensor CebR Is the gatekeeper of Streptomyces scabies pathogenicity. Mbio. 2015;6(2):e02018–14. doi: 10.1128/mBio.02018-1425714708
44. Tolonen AC, Chilaka AC, Church GM, Targeted gene inactivation in Clostridium phytofermentans shows that cellulose degradation requires the family 9 hydrolase Cphy3367. Mol Microbiol. 2009;74(6):1300–13. doi: 10.1111/j.1365-2958.2009.06890.x19775243
45. Beeson WT, Vu VV, Span EA, Phillips CM, Marletta MA, Cellulose degradation by polysaccharide monooxygenases. Annu Rev Biochem. 2015;84:923–46. doi: 10.1146/annurev-biochem-060614-03443925784051
46. Forsberg Z, Mackenzie AK, Sorlie M, Rohr AK, Helland R, Arvai AS, et al. Structural and functional characterization of a conserved pair of bacterial cellulose-oxidizing lytic polysaccharide monooxygenases. Proc Natl Acad Sci U S A. 2014;111(23):8446–51.
47. Forsberg Z, Vaaje-Kolstad G, Westereng B, Bunaes AC, Stenstrom Y, MacKenzie A, et al. Cleavage of cellulose by a CBM33 protein. Protein Sci. 2011;20(9):1479–83. doi: 10.1002/pro.68921748815
48. Vaaje-Kolstad G, Westereng B, Horn SJ, Liu ZL, Zhai H, Sorlie M, et al. An oxidative enzyme boosting the enzymatic conversion of recalcitrant polysaccharides. Science. 2010;330(6001):219–22. doi: 10.1126/science.119223120929773
49. Book AJ, Yennamalli RM, Takasuka TE, Currie CR, Phillips GN, JrFox BG, Evolution of substrate specificity in bacterial AA10 lytic polysaccharide monooxygenases. Biotechnol Biofuels. 2014;7:109.
50. Foreman PK, Brown D, Dankmeyer L, Dean R, Diener S, Dunn-Coleman NS, et al. Transcriptional regulation of biomass-degrading enzymes in the filamentous fungus Trichoderma reesei. J Biol Chem. 2003;278(34):31988–97. 12788920
51. Henrissat B, Cellulases and their interaction with cellulose. Cellulose. 1994;1(3):169–96.
52. Balows A, The Prokaryotes: A handbook on the biology of bacteria. 2nd ed. New York: Springer-Verlag; 1992.
53. Miller GL, Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem. 1959;31(3):426–8.
54. Teymouri F, Laureano-Perez L, Alizadeh H, Dale BE, Ammonia fiber explosion treatment of corn stover. Appl Biochem Biotechnol. 2004;113:951–63.
55. Schulein M, Enzymatic properties of cellulases from Humicola insolens. J Biotechnol. 1997;57(1–3):71–81.
56. Katoh K, Standley DM, MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability. Mol Biol Evol. 2013;30(4):772–80. doi: 10.1093/molbev/mst01023329690
57. Stamatakis A, RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014; 30(9):1312–3.
58. Kanehisa M, Sato Y, Morishima K, BlastKOALA and GhostKOALA: KEGG Tools for Functional Characterization of Genome and Metagenome Sequences. J Mol Biol. 2016; 428(4):726–31.
59. Edgar RC, MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32(5):1792–7. 15034147
60. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Hohna S, et al. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol. 2012;61(3):539–42. doi: 10.1093/sysbio/sys02922357727
61. Chen JQ, Weimer PJ, Competition among three predominant ruminal cellulolytic bacteria in the absence or presence of non-cellulolytic bacteria. Microbiology. 2001;147:21–30.
62. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, et al. Cytoscape: A software environment for integrated models of biomolecular interaction networks. Genome Res. 2003;13(11):2498–504. 14597658
63. Bailey TL, Williams N, Misleh C, Li WW, MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Res. 2006;34(Web Server issue):W369–73. 16845028
64. Grant CE, Bailey TL, Noble WS, FIMO: scanning for occurrences of a given motif. Bioinformatics. 2011;27(7):1017–8. doi: 10.1093/bioinformatics/btr06421330290
65. Wu M, Chatterji S, Eisen JA, Accounting for alignment uncertainty in phylogenomics. PLoS ONE. 2012;7(1):e30288. doi: 10.1371/journal.pone.003028822272325
66. Yang Z, PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci. 1997;13(5):555–6. 9367129
67. Roy A, Kucukural A, Zhang Y, I-TASSER: a unified platform for automated protein structure and function prediction. Nat Protoc. 2010;5(4):725–38. doi: 10.1038/nprot.2010.520360767
68. David LA, Alm EJ, Rapid evolutionary innovation during an Archaean genetic expansion. Nature. 2011;469(7328):93–6. doi: 10.1038/nature0964921170026
69. Price MN, Dehal PS, Arkin AP, FastTree 2—approximately maximum-likelihood trees for large alignments. PLoS ONE. 2010;5(3):e9490.
70. Tamura K, Battistuzzi FU, Billing-Ross P, Murillo O, Filipski A, Kumar S, Estimating divergence times in large molecular phylogenies. Proc Natl Acad Sci U S A. 2012;109(47):19333–8. doi: 10.1073/pnas.121319910923129628
71. Sambrook J, Russell DW, The condensed protocols from molecular cloning: a laboratory manual. Cold Spring Harbor: Cold Spring Harbor Laboratory Press; 2006.
72. Bierman M, Logan R, Obrien K, Seno ET, Rao RN, Schoner BE, Plasmid cloning vectors for the conjugal transfer of DNA from Escherichia coli to Streptomyces spp. Gene. 1992;116(1):43–9. 1628843
73. Madduri K, Kennedy J, Rivola G, Inventi-Solari A, Filippini S, Zanuso G, et al. Production of the antitumor drug epirubicin (4 '-epidoxorubicin) and its precursor by a genetically engineered strain of Streptomyces peucetius. Nat Biotechnol. 1998;16(1):69–74. 9447597
74. Galm U, Wendt-Pienkowski E, Wang LY, George NP, Oh TJ, Yi F, et al. The biosynthetic gene cluster of zorbamycin, a member of the bleomycin family of antitumor antibiotics, from Streptomyces flavoviridis ATCC 21892. Mol Biosyst. 2009;5(1):77–90.
75. Adams AS, Adams SM, Currie CR, Gillette NE, Raffa KF, Geographic variation in bacterial communities associated with the red turpentine beetle (Coleoptera: Curculionidae). Environ Entomol. 2010;39(2):406–14. doi: 10.1603/EN0922120388269
76. Adams AS, Aylward FO, Adams SM, Erbilgin N, Aukema BH, Currie CR, et al. Mountain pine beetles colonizing historical and naive host trees are associated with a bacterial community highly enriched in genes contributing to terpene metabolism. Appl Environ Microbiol. 2013;79(11):3468–75.
77. Carr G, Poulsen M, Klassen JL, Hou YP, Wyche TP, Bugni TS, et al. Microtermolides A and B from termite-associated Streptomyces sp. and structural revision of vinylamycin. Org Lett. 2012;14(11):2822–5. doi: 10.1021/ol301043p22591554
78. Grubbs KJ. Microbial communities associated with ambrosia beetles and the European honey bee, Apis mellifera. Ph.D. Thesis, University of Wisconsin—Madison. 2013. Available: https://search.library.wisc.edu/catalog/9910160552302121
79. Hanshew AS. Microbial ecology of tropical arboreal ants. Ph.D. Thesis, University of Wisconsin—Madison. 2013. Available: https://search.library.wisc.edu/catalog/9910190787102121
80. Poulsen M, Oh DC, Clardy J, Currie CR, Chemical analyses of wasp-associated Streptomyces bacteria reveal a prolific potential for natural products discovery. PLoS ONE. 2011;6(2):e16763.
81. Schwab L. Investigation of endosymbiotic Actinobacteria occurring in higher fungi and medicinal prairie plants. M.Sc. Thesis, University of Wisconsin—Madison. 2011.
82. Visser AA, Nobre T, Currie CR, Aanen DK, Poulsen M, Exploring the potential for Actinobacteria as defensive symbionts in fungus-growing termites. Microb Ecol. 2012;63(4):975–85. doi: 10.1007/s00248-011-9987-422173371