Identification of antibacterial peptides from endophytic microbiome

Applied Microbiology and Biotechnology

Volumn 100, Issue 21, 2016, Pages 9283-9293

  Tejesvi, M V ^a   Picart, P ^a,b   Kajula, M ^c   Hautajarvi H ^c   Ruddock, L ^a   Kristensen, H H ^d   Tossi, A ^e   Sahl, H G ^b   Ek, S ^a   Mattila, S ^a   Pirttila A M ^a  

^a UNIVERSITY OF OULU   (Finland)

^b UNIVERSITY OF BONN   (Germany)

^c Admescope Ltd   (Finland)

^d NOVOZYMES A S   (Denmark)

^e UNIVERSITY OF TRIESTE   (Italy)

Author keywords

Antimicrobial peptide; Endophyte; Microbiome; Unculturable

Indexed keywords

BACTERIA; BIODIVERSITY; CLONE CELLS; CLONING; ESCHERICHIA COLI; GENES; PEPTIDES; PROTEINS;

ANTI-BACTERIAL ACTIVITY; ANTI-MICROBIAL ACTIVITY; ANTIMICROBIAL PEPTIDE; ENDOPHYTE; MICROBIOME; NEXT-GENERATION SEQUENCING; PHARMACEUTICAL INDUSTRY; UNCULTURABLE;

MICROORGANISMS;

AMPICILLIN; CHLORAMPHENICOL; INTERNAL TRANSCRIBED SPACER 2; POLYPEPTIDE ANTIBIOTIC AGENT; TRANSCRIPTION FACTOR AP 1; ANTIINFECTIVE AGENT; PEPTIDE;

ANTIMICROBIAL ACTIVITY; BACTERIUM; BIOTECHNOLOGY; DRUG DEVELOPMENT; ENDOPHYTE; FUNGUS; GENE EXPRESSION; GENETIC RESOURCE; GENOME; MICROBIAL COMMUNITY; PEPTIDE; SHRUB;

ALPHA HELIX; AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ANTIBACTERIAL ACTIVITY; ARTICLE; CONTROLLED STUDY; DNA LIBRARY; DNA SEQUENCE; DRUG IDENTIFICATION; EMPETRUM NIGRUM; ENDOPHYTIC FUNGUS; ESCHERICHIA COLI; FOSMID; FUNGAL GENOME; FUSARIUM OXYSPORUM; GENE EXPRESSION; GENETIC RESOURCE; IN VITRO STUDY; MICROBIAL DIVERSITY; MICROBIOME; MINIMUM INHIBITORY CONCENTRATION; MOLECULAR CLONING; NEXT GENERATION SEQUENCING; NONHUMAN; NUCLEOTIDE SEQUENCE; PERENNIAL PLANT; PROMOTER REGION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; SHRUB; STAPHYLOCOCCUS AUREUS; VERTICILLIUM DAHLIAE; DRUG EFFECTS; ENDOPHYTE; ERICACEAE; FUNGUS; GENETIC SCREENING; GENETICS; METABOLISM; MICROBIOLOGY;

EMPETRUM NIGRUM; ESCHERICHIA COLI; STAPHYLOCOCCUS AUREUS;

ANTI-BACTERIAL AGENTS; ENDOPHYTES; ERICACEAE; ESCHERICHIA COLI; FUNGI; GENETIC TESTING; PEPTIDES; STAPHYLOCOCCUS AUREUS;

EID: 84982273161     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-016-7765-4     Document Type: Article

References (63)

1. Almaas H, Eriksen E, Sekse C, Comi I, Flengsrud R, Holm H, Jensen E, Jacobsen M, Langsrud T, Vegarud GE (2011) Antibacterial peptides derived from caprine whey proteins, by digestion with human gastrointestinal juice. Br J Nutr 106:896–905
2. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410
3. Amann RI, Ludwig W, Schleifer KH (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59:143–169
4. Andersen JH, Jenssen H, Sandvik K, Gutteberg TJ (2004) Anti-HSV activity of lactoferrin and lactoferricin is dependent on the presence of heparan sulphate at the cell surface. J Med Virol 74:262–271
5. Andersen AS, Sandvang D, Schnorr KM, Kruse T, Neve S, Joergensen B, Karlsmark T, Krogfelt KA (2010) A novel approach to the antimicrobial activity of maggot debridement therapy. J Antimicrob Chemother 65:1646–1654
6. Artimo P, Jonnalagedda M, Arnold K, Baratin D, Csardi G, de Castro E, Duvaud S, Flegel V, Fortier A, Gasteiger E, Grosdidier A, Hernandez C, Ioannidis V, Kuznetsov D, Liechti R, Moretti S, Mostaguir K, Redaschi N, Rossier G, Xenarios I, Stockinger H (2012) ExPASy: SIB bioinformatics resource portal. Nucleic Acids Res 40:W597–W603
7. Avrova A, Knogge W (2012) Rhynchosporium commune: a persistent threat to barley cultivation. Mol Plant Pathol 13:986–997
8. Balint M, Tiffin P, Hallstrom B, O'Hara RB, Olson MS, Fankhauser JD, Piepenbring M, Schmitt I (2013) Host genotype shapes the foliar fungal microbiome of balsam poplar (Populus balsamifera). PLoS One 8:e53987
9. Banik JJ, Brady SF (2010) Recent application of metagenomic approaches toward the discovery of antimicrobials and other bioactive small molecules. Curr Opin Microbiol 13:603–609
10. Bara R, Aly AH, Pretsch A, Wray V, Wang B, Proksch P, Debbab A (2013) Antibiotically active metabolites from Talaromyces wortmannii, an endophyte of Aloe vera. J Antibiot (Tokyo) 66:491–493
11. Baumann P (2005) Biology bacteriocyte-associated endosymbionts of plant sap-sucking insects. Annu Rev Microbiol 59:155–189
12. Boman HG (2003) Antibacterial peptides: basic facts and emerging concepts. J Intern Med 254:197–215
13. Brady SF (2007) Construction of soil environmental DNA cosmid libraries and screening for clones that produce biologically active small molecules. Nat Protoc 2:1297–1305
14. Buee M, Reich M, Murat C, Morin E, Nilsson RH, Uroz S, Martin F (2009) 454 pyrosequencing analyses of forest soils reveal an unexpectedly high fungal diversity. New Phytol 184:449–456
15. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, Fierer N, Knight R (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci U S A 108(Suppl 1):4516–4522
16. Cowan D, Meyer Q, Stafford W, Muyanga S, Cameron R, Wittwer P (2005) Metagenomic gene discovery: past, present and future. Trends Biotechnol 23:321–329. doi:10.1016/j.tibtech.2005.04.001
17. Duong LM, Jeewon R, Lumyong S, Hyde KD (2006) DGGE coupled with ribosomal DNA gene phylogenies reveal uncharacterized fungal phylotypes. Fungal Diversity 23:121–138
18. Emanuelsson O, Brunak S, von Heijne G, Nielsen H (2007) Locating proteins in the cell using TargetP, SignalP and related tools. Nat Protoc 2:953–971
19. Finn RD, Tate J, Mistry J, Coggill PC, Sammut SJ, Hotz HR, Ceric G, Forslund K, Eddy SR, Sonnhammer EL, Bateman A (2008) The Pfam protein families database. Nucleic Acids Res 36:D281–D288
20. Frank J, Crous PW, Groenewald JZ, Oertel B, Hyde KD, Phengsintham P, Schroers HJ (2010) Microcyclospora and Microcyclosporella: novel genera accommodating epiphytic fungi causing sooty blotch on apple. Persoonia 24:93–105
21. Fu J, Bian X, Hu S, Wang H, Huang F, Seibert PM, Plaza A, Xia L, Muller R, Stewart AF, Zhang Y (2012) Full-length RecE enhances linear-linear homologous recombination and facilitates direct cloning for bioprospecting. Nat Biotechnol 30:440–446
22. Galvao TC, Mohn WW, de Lorenzo V (2005) Exploring the microbial biodegradation and biotransformation gene pool. Trends Biotechnol 23:497–506
23. Geddy R, Brown GG (2007) Genes encoding pentatricopeptide repeat (PPR) proteins are not conserved in location in plant genomes and may be subject to diversifying selection. BMC Genomics 8:130
24. Gifford JL, Hunter HN, Vogel HJ (2005) Lactoferricin: a lactoferrin-derived peptide with antimicrobial, antiviral, antitumor and immunological properties. Cell Mol Life Sci 62:2588–2598
25. Hardoim PR, van Overbeek LS, Berg G, Pirttila AM, Compant S, Campisano A, Doring M, Sessitsch A (2015) The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol Mol Biol Rev 79:293–320
26. Higgins KL, Arnold AE, Miadlikowska J, Sarvate SD, Lutzoni F (2007) Phylogenetic relationships, host affinity, and geographic structure of boreal and arctic endophytes from three major plant lineages. Mol Phylogenet Evol 42:543–555
27. Hyde KD, Soytong K (2008) The fungal endophyte dilemma. Fungal Diversity 33:163–173
28. Ihrmark K, Bodeker IT, Cruz-Martinez K, Friberg H, Kubartova A, Schenck J, Strid Y, Stenlid J, Brandstrom-Durling M, Clemmensen KE, Lindahl BD (2012) New primers to amplify the fungal ITS2 region—evaluation by 454-sequencing of artificial and natural communities. FEMS Microbiol Ecol 82:666–677
29. Koljalg U, Nilsson RH, Abarenkov K, Tedersoo L, Taylor AF, Bahram M, Bates ST, Bruns TD, Bengtsson-Palme J, Callaghan TM, Douglas B, Drenkhan T, Eberhardt U, Duenas M, Grebenc T, Griffith GW, Hartmann M, Kirk PM, Kohout P, Larsson E, Lindahl BD, Lucking R, Martin MP, Matheny PB, Nguyen NH, Niskanen T, Oja J, Peay KG, Peintner U, Peterson M, Poldmaa K, Saag L, Saar I, Schussler A, Scott JA, Senes C, Smith ME, Suija A, Taylor DL, Telleria MT, Weiss M, Larsson KH (2013) Towards a unified paradigm for sequence-based identification of fungi. Mol Ecol 22:5271–5277
30. Koskimäki JJ, Nylund S, Suorsa M, Pirttilä AM (2010) Mycobacterial endophytes are enriched during micropropagation of Pogonatherum paniceum. environmental microbiology reports 2:619–624
31. Kusari S, Zuhlke S, Spiteller M (2011) Effect of artificial reconstitution of the interaction between the plant Camptotheca acuminata and the fungal endophyte Fusarium solani on camptothecin biosynthesis. J Nat Prod 74:764–775
32. Ling LL, Schneider T, Peoples AJ, Spoering AL, Engels I, Conlon BP, Mueller A, Schaberle TF, Hughes DE, Epstein S, Jones M, Lazarides L, Steadman VA, Cohen DR, Felix CR, Fetterman KA, Millett WP, Nitti AG, Zullo AM, Chen C, Lewis K (2015) Erratum: A new antibiotic kills pathogens without detectable resistance. Nature 520:388
33. Lorenz P, Liebeton K, Niehaus F, Eck J (2002) Screening for novel enzymes for biocatalytic processes: accessing the metagenome as a resource of novel functional sequence space. Curr Opin Biotechnol 13:572–577
34. Martin F, Cullen D, Hibbett D, Pisabarro A, Spatafora JW, Baker SE, Grigoriev IV (2011) Sequencing the fungal tree of life. New Phytol 190:818–821
35. McCutcheon AR, Stokes RW, Thorson LM, Ellis SM, Hancock REW, Towers GHN (1997) Anti-mycobacterial screening of british columbian medicinal plants. Pharmaceutical Biology 35:77–83
36. Mitchell AM, Strobel GA, Hess WM, Vargas PN, Ezra D (2008) Muscodor crispans, a novel endophyte from Ananas ananassoides in the Bolivian Amazon. Fungal Diversity 31:37–43
37. National Research Council (US) (2007) Committee on Metagenomics. In: Challenges and functional applications
38. Nikolcheva LG, Bärlocher F (2004) Taxon-specific fungal primers reveal unexpectedly high diversity during leaf decomposition in a stream. Mycological Progress 3:41–49
39. Ondov BD, Bergman NH, Phillippy AM (2011) Interactive metagenomic visualization in a Web browser. BMC Bioinformatics 12:385-2105–3812-385
40. Owen JG, Robins KJ, Parachin NS, Ackerley DF (2012) A functional screen for recovery of 4-phosphopantetheinyl transferase and associated natural product biosynthesis genes from metagenome libraries. Environ Microbiol 14:1198–1209
41. Park SH, Cheong DE, Lee JY, Han SS, Lee JH, Kim GJ (2007) Analyses of the structural organization of unidentified open reading frames from metagenome. Biochem Biophys Res Commun 356:961–967
42. Petersen TN, Brunak S, von Heijne G, Nielsen H (2011) Signal P 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8:785–786
43. Pirttilä AM, Kämäräinen T, Hirsikorpi M, Jaakola L, Hohtola A (2001) DNA isolation methods for medicinal and aromatic plants. Plant molecular biology report 19: a-f
44. Saha D, Prasad AM, Srinivasan R (2007) Pentatricopeptide repeat proteins and their emerging roles in plants. Plant Physiol Biochem 45:521–534
45. Salanoubat M, Genin S, Artiguenave F, Gouzy J, Mangenot S, Arlat M, Billault A, Brottier P, Camus JC, Cattolico L, Chandler M, Choisne N, Claudel-Renard C, Cunnac S, Demange N, Gaspin C, Lavie M, Moisan A, Robert C, Saurin W, Schiex T, Siguier P, Thebault P, Whalen M, Wincker P, Levy M, Weissenbach J, Boucher CA (2002) Genome sequence of the plant pathogen Ralstonia solanacearum. Nature 415:497–502
46. Schloss PD, Handelsman J (2003) Biotechnological prospects from metagenomics. Curr Opin Biotechnol 14:303–310
47. Schneider T, Kruse T, Wimmer R, Wiedemann I, Sass V, Pag U, Jansen A, Nielsen AK, Mygind PH, Raventos DS, Neve S, Ravn B, Bonvin AM, De Maria L, Andersen AS, Gammelgaard LK, Sahl HG, Kristensen HH (2010) Plectasin, a fungal defensin, targets the bacterial cell wall precursor Lipid II. Science 328:1168–1172
48. Schulz B, Boyle C (2005) The endophytic continuum. Mycol Res 109:661–686
49. Seena S, Wynberg N, Bärlocher F (2008) Fungal diversity during leaf decomposition in a stream assessed through clone libraries. Fungal Diversity 30:1–14
50. Sessitsch A, Hardoim P, Doring J, Weilharter A, Krause A, Woyke T, Mitter B, Hauberg-Lotte L, Friedrich F, Rahalkar M, Hurek T, Sarkar A, Bodrossy L, van Overbeek L, Brar D, van Elsas JD, Reinhold-Hurek B (2012) Functional characteristics of an endophyte community colonizing rice roots as revealed by metagenomic analysis. Mol Plant Microbe Interact 25:28–36
51. Shang D, Sun Y, Wang C, Ma L, Li J, Wang X (2012) Rational design of anti-microbial peptides with enhanced activity and low cytotoxicity based on the structure of the arginine/histidine-rich peptide, chensinin-1. J Appl Microbiol 113:677–685
52. Shin K, Yamauchi K, Teraguchi S, Hayasawa H, Tomita M, Otsuka Y, Yamazaki S (1998) Antibacterial activity of bovine lactoferrin and its peptides against enterohaemorrhagic Escherichia coli O157:H7. Lett Appl Microbiol 26:407–411
53. Silphaduang U, Hincke MT, Nys Y, Mine Y (2006) Antimicrobial proteins in chicken reproductive system. Biochem Biophys Res Commun 340:648–655
54. Studier FW, Rosenberg AH, Dunn JJ, Dubendorff JW (1990) Use of T7 RNA polymerase to direct expression of cloned genes. Methods Enzymol 185:60–89
55. Tejesvi MV, Ruotsalainen AL, Markkola AM, Pirttilä AM (2010) Root endophytes along a primary succession gradient in Northern Finland. Fungal Diversity 41:125–134
56. Thevenet P, Shen Y, Maupetit J, Guyon F, Derreumaux P, Tuffery P (2012) PEP-FOLD: an updated de novo structure prediction server for both linear and disulfide bonded cyclic peptides. Nucleic Acids Res 40:W288–W293
57. Travadon R, Lawrence DP, Rooney-Latham S, Gubler WD, Wilcox WF, Rolshausen PE, Baumgartner K (2015) Cadophora species associated with wood-decay of grapevine in North America. Fungal Biol 119:53–66
58. Turnbaugh PJ, Gordon JI (2008) An invitation to the marriage of metagenomics and metabolomics. Cell 134:708–713
59. Unterseher M, Jumpponen A, Opik M, Tedersoo L, Moora M, Dormann CF, Schnittler M (2011) Species abundance distributions and richness estimations in fungal metagenomics—lessons learned from community ecology. Mol Ecol 20:275–285
60. van Lith M, Karala AR, Bown D, Gatehouse JA, Ruddock LW, Saunders PT, Benham AM (2007) A developmentally regulated chaperone complex for the endoplasmic reticulum of male haploid germ cells. Mol Biol Cell 18:2795–2804
61. Whitman WB, Coleman DC, Wiebe WJ (1998) Prokaryotes: the unseen majority. Proc Natl Acad Sci U S A 95:6578–6583
62. Wild J, Hradecna Z, Szybalski W (2002) Conditionally amplifiable BACs: switching from single-copy to high-copy vectors and genomic clones. Genome Res 12:1434–1444
63. Zgoda JR, Porter JR (2001) A convenient microdilution method for screening natural products against bacteria and fungi. Pharmaceutical Biology 39:221–225