Ancient Bacteria–Amoeba Relationships and Pathogenic Animal Bacteria Joan E
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Washington University in St. Louis Washington University Open Scholarship Biology Faculty Publications & Presentations Biology 5-2-2017 Ancient bacteria–amoeba relationships and pathogenic animal bacteria Joan E. Strassmann Washington University in St Louis, [email protected] Longfei Shu Follow this and additional works at: https://openscholarship.wustl.edu/bio_facpubs Part of the Bacteriology Commons, Biology Commons, and the Environmental Microbiology and Microbial Ecology Commons Recommended Citation Strassmann, Joan E. and Shu, Longfei, "Ancient bacteria–amoeba relationships and pathogenic animal bacteria" (2017). Biology Faculty Publications & Presentations. 136. https://openscholarship.wustl.edu/bio_facpubs/136 This Article is brought to you for free and open access by the Biology at Washington University Open Scholarship. It has been accepted for inclusion in Biology Faculty Publications & Presentations by an authorized administrator of Washington University Open Scholarship. For more information, please contact [email protected]. PRIMER Ancient bacteria±amoeba relationships and pathogenic animal bacteria Joan E. Strassmann*, Longfei Shu Department of Biology, Washington University in St. Louis, St. Louis, Missouri, United States of America * [email protected] Abstract Long before bacteria infected humans, they infected amoebas, which remain a potentially important reservoir for human disease. Diverse soil amoebas including Dictyostelium and Acanthamoeba can host intracellular bacteria. Though the internal environment of free-living amoebas is similar in many ways to that of mammalian macrophages, they differ in a num- a1111111111 ber of important ways, including temperature. A new study in PLOS Biology by Taylor-Mul- a1111111111 neix et al. demonstrates that Bordetella bronchiseptica has two different gene suites that are a1111111111 activated depending on whether the bacterium finds itself in a hot mammalian or cool a1111111111 amoeba host environment. This study specifically shows that B. bronchiseptica not only a1111111111 inhabits amoebas but can persist and multiply through the social stage of an amoeba host, Dictyostelium discoideum. OPEN ACCESS Citation: Strassmann JE, Shu L (2017) Ancient Environmental amoebas came before animals as hosts to bacteria bacteria±amoeba relationships and pathogenic animal bacteria. PLoS Biol 15(5): e2002460. The bacteria that most concern us are those that make us sick, but we are sometimes so preoc- https://doi.org/10.1371/journal.pbio.2002460 cupied with our battle with them that we forget they have been waging a much longer war. 9 Published: May 2, 2017 More than a billion (10 ) years before the first animals, bacteria were evolving strategies first to resist being killed by protozoan predators and then to actually infect their former predators Copyright: © 2017 Strassmann, Shu. This is an open access article distributed under the terms of [1]. These strategies are likely to have laid the groundwork for the later evolution of animal± the Creative Commons Attribution License, which bacteria interactions, so understanding how they function provides an essential context for permits unrestricted use, distribution, and understanding modern-day bacterial pathogens in humans. This is particularly true for the reproduction in any medium, provided the original bacteria that invade animals through macrophages [2]. Further, environmental amoebas are author and source are credited. still ubiquitous in modern soil and water, so they may act as important reservoirs from which Funding: The authors received no specific funding emerging human diseases can arise [3]. Many amoebas, including Acanthamoeba castellanii, for this work. D. discoideum, Hartmannella vermiformis, and Naegleria gruberi, have been found to harbor Competing interests: The authors have declared bacteria [4]. Bacteria that can defeat amoebas' defenses gain a refuge in which to proliferate, that no competing interests exist. where they are protected from hostile external conditions by their unwitting hosts [5±8]. Abbreviations: LCV, Legionella-containing vacuole; It is worth pointing out that amoebas do not fall into a monophyletic group but instead NCBI, National Center for Biotechnology share a life form and a diet based on phagocytosis. The bacteria that can evade amoeba Information; T2SS, type II secretion system; T4SS, defenses are called amoeba-resistant bacteria [3,4]. In these amoebas, resistant bacteria can type IV secretion system. survive, proliferate, and be protected in adverse situations, particularly when the host amoeba Provenance: Commissioned; externally peer forms a hardy cyst with the bacteria inside. reviewed. PLOS Biology | https://doi.org/10.1371/journal.pbio.2002460 May 2, 2017 1 / 8 Glossary Amoeba-resistant bacteria: Bacteria that have evolved to resist being killed by free-liv- ing amoebas. Bacterial secretion system: The mechanisms by which bacterial pathogens evolved to export various virulence factors across the phospholipid membrane and cell envelope. Ejectosome: A peripheral cellular organelle responsible for ejecting cytosolic bacteria from the cell without lysing that cell. Fruiting body: A multicellular structure on which spore-producing structures are borne. Free-living amoebas: Widely distributed protozoa that have the ability to alter their shape and feed on bacteria, algae, fungi, and small organic particles. Lysosome: A membrane-bound organelle that contains hydrolytic enzymes that can break down biomolecules. Phagocytosis: The process by which a cell engulfs a solid particle to form an internal compartment known as a phagosome. Phagosome: A vacuole formed around a particle engulfed by phagocytosis. Symbiosis: A relationship between individuals of different species that live closely together. Two-component regulatory system: One kind of mechanism of signal transduction that allows organisms to sense and respond to a changing environment. Spore: A unit of sexual or asexual reproduction that is able to disperse and survive in unfavorable conditions. Virulence factor: Molecules produced by pathogens that can increase their fitness in interactions with the host. Survival strategies of intracellular bacteria within amoebas Entry of bacteria into amoebas is simple because amoebas eat bacteria. Amoebas normally engulf food bacteria by phagocytosis and kill them inside the phagosome, where ingested bac- teria are confronted with acidification, oxidative stress, nutrient deprivation, and various anti- microbial small molecules [2] [9,10]. Amoeba grazing has been suggested to be one of the major forces shaping bacterial abundance and diversity [11]. However, some bacteria have developed strategies to survive phagocytosis by amoebas and are able to exploit host cell resources. Bacteria like Legionella pneumophila that remain in the vacuole of macrophages in humans are perhaps the best-studied bacteria that infect humans and amoebas, but they are by no means the only ones (Table 1) [12,13]. The most obvious strategy to avoid being killed by the amoeba host is to escape from its vac- uole into the cytosol of the amoeba (Fig 1A). For example, M. marinum and M. tuberculosis have evolved this ability (Fig 1A, yellow). This process requires the mycobacterial type VII secretion system ESX-1 [12]. In addition, both M. marinum and M. tuberculosis can eject from the cell through an F-actin structure called an ejectosome and then spread from cell to cell [19,20]. In general, the cytosol is considered to be favorable for bacterial growth because it pro- vides nutrients and is isolated from the host immune system [21]. Therefore, it is an ideal place for bacteria to thrive after escaping from the phagosome. Some intracellular patho- gens can invade a more unusual intracellular niche: the eukaryotic nucleus (Fig 1A, green). PLOS Biology | https://doi.org/10.1371/journal.pbio.2002460 May 2, 2017 2 / 8 Table 1. List of human pathogens that are found in free-living amoebas. These bacteria are isolated from various amoeba hosts and have different life- styles [8,14±16]. They have evolved sophisticated ways to export various virulence factors across their bacterial inner and sometimes outer membrane (in gram-negative bacteria), as well as through the host plasma membrane or phagosomal membrane, by using diverse secretion systems [17,18]. Bacteria Amoeba hosts Location in Bacterial secretion systems known to be Human diseases amoebas present β proteobacteria Burkholderia cepacia Acanthamoeba Extracellular Type III secretion system; type VI secretion Pneumonia system Bu. pseudomallei Acanthamoeba Extracellular Type III secretion system; type VI secretion Melioidosis system Burkholderia spp. Dictyostelium Facultative Unknown Unknown intracellular γ proteobacteria Coxiella burnetii Acanthamoeba Obligate Dot/Icm type IVB secretion system Q fever intracellular Escherichia coli O157 Acanthamoeba Extracellular Type III secretion system; Tat secretion Hemorrhagic diarrhea; kidney pathway failure Francisella tularensis Acanthamoeba Facultative Type VI secretion system Tularemia intracellular L. pneumophila Various amoebas Facultative Type II secretion system; type IV secretion Legionnaires disease intracellular system; Tat secretion pathway L. anisa Acanthamoeba Facultative Unknown Pontiac fever; Legionnaires intracellular disease Pseudomonas Acanthamoeba Extracellular Tat secretion pathway; Type VI secretion Infect human cells aeruginosa system Vibrio cholerae Acanthamoeba, Extracellular Type I secretion