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Danielbarrosortegatese2019.Pdf Figure 1 Average biomass of Paenibacillus elgii strain AC13 cultures at 37°C expressing swarming or non-swarming behavior.Pró- CulturesReitoria were scraped Acadêmica from agar and weighted (n=147).......... 58 Escola de Saúde e Medicina Programa de Pós-Graduação Stricto Sensu em Ciências Genômicas e Biotecnologia Production of Polypeptin A analogues by Paenibacillus elgii strain AC13 and quorum sensing dependent bacterial processes Autor: Daniel Barros Ortega Orientadora: Cristine Chaves Barreto Brasília - DF 1 2019 Daniel Barros Ortega Production of Polypeptin A analogues by Paenibacillus elgii strain AC13 and quorum sensing dependent bacterial processes Tese apresentada ao Programa de Pós- graduação Stricto Sensu em Ciências Genômicas e Biotecnologia da Universidade Católica de Brasília como requisito parcial para obtenção do Título de Doutor em Ciências Genômicas e Biotecnologia Orientadora: Prof.ª Dr.ª Cristine Chaves Barreto Coordenadora: Prof.ª Dr.ª Maria Sueli Soares Felipe Brasília 2019 2 Para o Léo, João, Raissa, Nez e Neusa. Amo vocês. 3 AGRADECIMENTOS À Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, CAPES, pelo financiamento prestado; À Universidade Católica de Brasília e aos professores, por acreditarem em novas Ideias e no desenvolvimento da Pesquisa; À professora Dra. Beatriz Simas Magalhães, por ter me apresentado ao Projeto; À professora Dra. Cristine Chaves Barreto, por, apesar de tantas divergências, conseguiu aparar arestas e me ajudou a produzir este documento; À coordenação do programa de pós-graduação da UCB, pela compreensão e apoio; À Universidade da Califórnia San Diego e aos membros do Laboratório do Professor Dorrestein, pelas palestras, disponibilização do espaço e equipamentos; Aos amigos desde a infância até agora e colegas de laboratório Tamires, Clarissa, Rosiane, Flávio, Michel, Marise, Thiago entre tantos que compartilharam momentos de planejamento, organização, frustrações, conquistas e também de bem estar e insights, dos mais coerentes aos mais absurdos! Fundamentais. À minha mãe, Neusa; irmã, Raissa; e à Nez, pelo Todo. Aos meus sobrinhos, por serem a luz que ilumina tanto espaço e tempo deste Todo. 4 “Awareness is the world's mystical experience.” Thus Spoke Zarathustra; F. Nietzsche 5 Resumo Quorum sensing (QS) são sofisticadas redes de comunicação baseadas em trocas metabólicas que influenciam processos bacterianos como a bioluminescência, reprodução, esporulação, formação de biofilme, expressão de virulência e produção de antimicrobianos. Peptídeos não ribossomais (NRP) utilizam aminoácidos não proteinogênicos como blocos de construção, aumentando o número de possíveis arcabouços quando comparados aos obtidos pelo processo de síntese ribossômica. Naturalmente produzida por Paenibacillus elgii, a família das Pelgipeptinas (PGP) é constituída por cinco NRP cíclicos e catiônicos compostos por nove aminoácidos e uma cadeia de ácido graxo. Após a linearização de NRP semelhantes às PGP, concentrações mais baixas foram suficientes para inibição do crescimento de Candida albicans patogênica, ampliando a polivalência deste grupo de moléculas. A cepa de P. elgii AC13 foi isolada de amostras de solo do Cerrado brasileiro. PGP produzidas por AC13 tiveram atividade contra Escherichia coli, Staphylococcus aureus e Klebsiella pneumoniae multirresistente. Isoformas lineares de PGP também foram encontradas em culturas de AC13 em caldo nutriente. Parâmetros de crescimento, quantificação de PGP e caracterização parcial de lipopeptídeos produzidos sugerem que a cepa AC13 é capaz de modular a produção PGP em função de variações de seu ambiente ou de sua população inicial. Associações por Redes Moleculares indicam que o íon de massa 1.101,7052 Da (PGP- B) relaciona-se ao gene leu B, responsável por codificar 3-isopropilmalato desidrogenase em P. dendritiformis C454, P. selenitireducens, P. yonginensis e P. amylolyticus. A enzima é parte da via biossintética da leucina e é responsável por catalisar a oxidação do 3- isopropilmalato. Analises semelhantes também sugerem que a enzima responsável por sintetizar O-acetil-L-homoserina em Lysinibacillus sp. cepa FJAT-14222 está relacionada ao íon 416.7368 Da, ambos encontrados em cultura de AC13 por LC-MS. Entre as vias de sinalização de QS, N-acil-homoserina lactonas são moléculas de sinalização para mais de 70 espécies diferentes de bactérias Gram-negativas. Como forma de se aumentar as estratégias no combate aos microrganismos multirresistentes, sugere-se a interferência nos sistemas de comunicação QS, que podem ser interrompidos pela redução da atividade ou bloqueio da síntese de proteínas receptoras de sinalização ou ainda por meio de moléculas sintéticas análogas aos compostos sinalizadores de QS. Contudo, uma melhor compreensão da interface entre a biologia de sistemas e técnicas avançadas de redes moleculares se faz necessária. 6 Palavras-chave: Paenibacillus; Pelgipeptinas; microbiologia de solos; quorum-sensing Abstract Quorum sensing (QS) are sophisticated communication networks based on metabolic exchanges that influence bacteria processes such as reproduction, sporulation, biofilm formation, virulence and antimicrobials expression. Non-ribosomal peptides (NRP) use non- proteinogenic amino acids as building blocks, which increase the number of possible templates when compared to standard ribosomal synthesis process. Naturally produced by Paenibacillus elgii, the NRP family of Pelgipeptins (PGP) consists of five cyclic and cationic lipopeptides comprising nine amino acids and a fatty acid chain. Linearization of NRP similar to PGPs have improved antifungal activity against pathogenic Candida albicans. Paenibacillus elgii strain AC13 was isolated from soil samples of the Brazilian Cerrado. PGPs produced by AC13 were active against Escherichia coli, Staphylococcus aureus and multidrug resistant Klebsiella pneumoniae. Strain AC13 also synthesizes linear counterparts or PGPs in nutrient broth. Growth parameters, PGPs quantification, and partial characterization of produced lipopeptides suggest that strain AC13 is able to modulate its lipopeptides production based on variations of its environment or initial population. Molecular networking analysis indicates that the precursor mass of 1,101.7052 Da (PGP-B) is connected to the gene leuB pathway, responsible to code 3-isopropylmalate dehydrogenase described for P. dendritiformis C454, P. selenitireducens, P. yonginensis and P. amylolyticus. The enzyme is part of leucine biosynthetic pathway and is responsible to catalyze the oxidation of 3-isopropylmalate. Molecular networking analysis also indicates that the enzyme responsible to synthesize O-acetyl-L-homoserine (gene metAA) expressed by Lysinibacillus sp. strain FJAT-14222 is connected to precursor mass 416.7368 Da. Among QS signaling pathways, N-acyl-homoserine lactones occur as signaling molecules for more than 70 different species of diderm bacteria. QS communication can be interrupted by reducing the activity of signaling receptor proteins, their synthesis or by synthetic molecules analogous to QS signaling compounds, increasing the strategies on fighting against multidrug resistant microorganisms. Notwithstanding, a better understanding of the overlap between system biology and advanced molecular network techniques is needed. Key-words: Paenibacillus; Pelgipeptin; soil microbiology; quorum-sensing. 7 List of Abbreviations QS – Quorum Sensing; NRP – Non ribosomal peptides; PGP – Pelgipeptin; AHL – Acyl-homoserine lactones; AIP – Auto-inducing peptides; RNA – Ribonucleic acid; DNA – Deoxyribonucleic acid; EPS – Extracellular polymeric substances; GMP – Guanosine 3’, 5’-monophosphate; NRPS – Nonribosomal Peptide Synthases; LC – Liquid Chromatography; MS – Mass Spectrometry; rRNA – ribosomal RNA; SDS – Sodium dodecyl sulfate; PGAP – Prokaryotic Genome Annotation Process Pipeline; NCBI – National Center for Biotechnology Information; PGAAP – Prokaryotic Genome Automatic Annotation Pipeline; ORF – Open reading frame; HMM – Hidden Markov model; CDS – Coding sequences; tRNA – transporter RNA; ANI – Average Nucleotide Identity; MALDI-TOF – Matrix assisted laser desorption ionization time of flight; RP-HPLC – Reversed-Phase High Performance Liquid Chromatography; UPLC – Ultra Performance Liquid Chromatography; SG – Schaeffer’s Glucose; ACN – Acetonitrile; MMP – Mineral Medium for Paenibacillus; NB – Nutrient Broth; MHB – Mueller-Hinton Broth; PMHB – Peptone enriched Mueller-Hinton broth; 8 OD – Optical density; SASPs – Small acid-soluble proteins; NPAAs – Non-proteinogenic amino acids; Dab – 2, 4-diaminobutyric acid; Val – Valine Ile – Isoleucine. Phe – Phenylalanine; Leu – Leucine; Ser – Serine; AFB – American Foulbrood disease; GNPS – Global Natural Products Social Molecular Networking; LB – Luria-Bertani; CFU – Colony forming units; RT – Retention time; MDR – Multidrug resistant; TFA – Trifluoroacetic acid; MIC – Minimal Inhibitory concentration; FIC – Fractional Inhibitory Concentration; FICI – Fractional Inhibitory Concentration Index; UV – Ultraviolet; MTT – 3-[4,5-dimethylthiazol-2-yl]-2, 5-diphenyltetrazolium bromide; TSA – Trypticase soy agar; ATCC – American Type Culture Collection; 9 List of Figures Introduction………………………………………………………………………………....................19 Figure 1: LuxIR bioluminescence expression system for Vibrio fischeri represented as quorum sensing mechanism model for diderm bacteria. Protein luxI is responsible to synthesizes auto-inducers (AHL). At high cell density, a critical threshold of auto-inducers triggers a
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