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Pedro Manuel Duarte Monteiro Pedro Manuel Duarte Monteiro FIGHTING THE RESISTANCE: ALGAE AS KEY ORGANISMS AGAINST ANTIBACTERIAL RESISTANCE AN OVERVIEW OF RESISTANCE MECHANISMS, ALGAE COMPOUNDS AND COMMERCIAL CHALLENGES Outubro 2020 Pedro Manuel Duarte Monteiro FIGHTING THE RESISTANCE: ALGAE AS KEY ORGANISMS AGAINST ANTIBACTERIAL RESISTANCE AN OVERVIEW OF RESISTANCE MECHANISMS, ALGAE COMPOUNDS AND COMMERCIAL CHALLENGES Dissertação no âmbito do Mestrado em Biologia celular e molecular orientada pela Professora Doutora Gabriela Conceição Duarte Jorge da Silva e pela Professora Doutora Paula Maria de Melim Vasconcelos de Vitorino Morais e apresentada ao Departamento de Ciências da Vida da Faculdade de Ciências e Tecnologia da Universidade de Coimbra Outubro 2020 Agradecimentos/Acknowledgments No percurso desta dissertação, é imprescindível agradecer o apoio da minha orientadora Professora Gabriela Jorge e da minha co- orientadora Professora Paula Morais, pela oportunidade que me foi dada e pela paciência demonstrada comigo na elaboração deste trabalho. Gostaria também de agradecer ao Professor Leonel Pereira e ao meu colega João Cotas, pela disponibilidade constante durante este projeto. Aos meus pais, pelo apoio incondicional que me permitiu chegar onde estou agora. Aos meus amigos, pelo suporte incansável durante este trabalho. À Sara, pela força constante. Muito obrigado a todos. iii Index Acknowledgments… ..................................................................................... iii Index… ......................................................................................................... iv Image Index................................................................................................. vi/vii Abbreviations................................................................................................ viii Resumo/abstract ........................................................................................ ix/xi The antibacterial resistance problem ............................................................ 12 How far has antibacterial (ABR) spread ............................................. 14 key-messages .................................................................................... 17 Resistance mechanisms: Efficiency at its finest ........................................... 18 Conventional mechanisms of resistance ............................................ 19 Mutational alteration of target protein ...................................... 19 Enzymatic inactivation of drug ................................................. 20 Aminoglycosides ........................................................... 20 Beta-lactams ................................................................. 20 Acquisition of genes from other species .................................. 21 Bypassing the target ................................................................ 21 Preventing drug access to targets ........................................... 22 Local inhibition of drug access ...................................... 22 Non-specific inhibition of drug access ........................... 22 Drug specific efflux pumps ............................................ 22 The biofilm structure: Elegant evolution ............................................. 23 Bacterial adhesion: the first step ............................................. 25 Biofilm maturation .................................................................... 28 Extracellular DNA .................................................................... 30 Quorum sensing ...................................................................... 31 Relationship between biofilm formation and disease .......................... 33 Tolerance and persistence of biofilm structures ....................... 35 Other physiological changes due to biofilm mode of growth .................................................................................... 38 key-messages .................................................................................... 40 A blue approach: Seeking solutions from aquatic iv environments… ............................................................................................ 41 Macroalgae: multicellular aquatic flora ............................................... 42 Microalgae:Microscopic factories ....................................................... 43 Cyanobacteria: Where it all started ..................................................... 44 Compounds produced by algae ......................................................... 45 Carbohydrates ......................................................................... 45 Amino acids and peptides ....................................................... 48 Lectins ..................................................................................... 49 Lipids, fatty acids and sterols .................................................. 50 Pigments ................................................................................. 53 Vitamins and minerals ............................................................. 54 Secondary metabolites ............................................................ 55 Phenols ......................................................................... 55 Phenolic acids ............................................................... 55 Phlorotannins ................................................................ 57 Bromophenols............................................................... 58 Flavonoids .................................................................... 59 Phenolic terpenoids ...................................................... 60 Mycosporine-like aminoacids (MAAs) ........................... 61 Non-phenolic secondary metabolites ...................................... 62 Terpenes ...................................................................... 62 Alkaloids ....................................................................... 62 Halogenated compounds .............................................. 63 Key messages ............................................................. 63 Can algae solutions contribute to resistance mitigation? ............................. 64 Algae compounds with antibacterial action ................................ 64 Algae compounds in biosynthesis of nanoparticles ................... 69 On conventional and current methods for extraction ................. 70 Key-messages .......................................................................... 73 Conclusion ................................................................................................... 74 References ................................................................................................... 76 v Image index Figure 1- Transmission of bacterial organisms (pathogenic or commensal) to humans ............................................................................................................ 15 Figure 2- Mechanisms of resistance and implications in foodborne disease ............................................................................................................. 16 Figure 3- Resistance acquisition and consequent mechanisms expressed by resistant organisms .......................................................................................... 18 Figure 4- Biofilm formation is characterized by sequential mechanisms triggered by environmental factors and environment bacteria are. These steps begin with adhesion to a substrate, formation of microcolonies through aggregation, maturation and finally dispersal, in order to colonize other surfaces ............................................................................................................24 Figure 5- Biofilm attachment and molecular mechanisms of adhesion. (A)- Pseudomonas aeruginosa; (B)-Escherichia coli, (C)-Vibrio cholerae ........................................................................................................... 27 Figure 6- Maturation and bacterial organization in Vibrio cholerae biofilms forming the characteristically towers. (A) represents a cross-section of the bottom layer of a 18h V. cholerae biofilm, and the corresponding image in (B), demonstrating color coding for Z position. (C) representation of steps involved in V. cholerae biofilm formation. Yellow represents bacterial cells and pink the EPS matrix. (D) Side views of 7-h-old biofilms grown with 0.4 mg/mL A22, magenta; without treatment. Yellow; and with 4 mg/mL cefalexin, cyan. A22 and cefalexin cause the cells to become shorter and longer, respectively ...................................................................................................... 29 Figure 7- Overview of the major antimicrobial resistance and tolerance mechanisms employed by bacterial biofilms. Biofilm cells (yellow rectangles) are embedded in the EPS matrix (shown in green). The biofilm is attached to a surface (grey rectangle), biotic or abiotic. Resistance mechanisms are numbered as follows: (1) nutrient gradient (color-intensity gradient) with less nutrient availability in the core of the biofilm, (2) matrix exopolysaccharides, (3) extracellular DNA, (4) stress responses (oxidative stress response, stringent vi response, etc.), (5) discrete genetic determinants that are specifically expressed in biofilms and whose gene products act to reduce biofilm susceptibility via diverse mechanisms (ndvB, brlR, etc.), (6) multidrug efflux pumps, (7) intercellular interactions (horizontal gene transfer, quorum sensing, multispecies
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