Research Article: Ancient bacteria–amoeba relationships and pathogenic animal bacteria

Date Published: May 2, 2017

Publisher: Public Library of Science

Author(s): Joan E. Strassmann, Longfei Shu

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 number of important ways, including temperature. A new study in PLOS Biology by Taylor-Mulneix et al. demonstrates that Bordetella bronchiseptica has two different gene suites that are activated depending on whether the bacterium finds itself in a hot mammalian or cool amoeba host environment. This study specifically shows that B. bronchiseptica not only inhabits amoebas but can persist and multiply through the social stage of an amoeba host, Dictyostelium discoideum.

Partial Text: The bacteria that most concern us are those that make us sick, but we are sometimes so preoccupied with our battle with them that we forget they have been waging a much longer war. More than a billion (109) 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 [1]. These strategies are likely to have laid the groundwork for the later evolution of animal–bacteria interactions, so understanding how they function provides an essential context for understanding modern-day bacterial pathogens in humans. This is particularly true for the bacteria that invade animals through macrophages [2]. Further, environmental amoebas are still ubiquitous in modern soil and water, so they may act as important reservoirs from which emerging human diseases can arise [3]. Many amoebas, including Acanthamoeba castellanii, D. discoideum, Hartmannella vermiformis, and Naegleria gruberi, have been found to harbor bacteria [4]. Bacteria that can defeat amoebas’ defenses gain a refuge in which to proliferate, where they are protected from hostile external conditions by their unwitting hosts [5–8].

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 bacteria are confronted with acidification, oxidative stress, nutrient deprivation, and various antimicrobial 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].

We began this piece by noting that amoebas antedated animals on the planet by more than a billion years. If bacteria began their infectious lives in soil and water, then we expect those lineages to be more ancient than those from animals. There is a comprehensive and recent study on this topic for B. bronchiseptica, which is a bacterium in the gram-negative Betaproteobacteria [35]. It causes respiratory infections in some species of mammals and is closely related to B. pertussis, which causes whooping cough in humans, accounting for about 89,000 deaths worldwide in 2008, according to the World Health Organization.

As McFall-Ngai and coauthors so nicely put it, animals evolved in a world that already contained billions of bacteria, archaea, and amoebas [38]. Thus, it is no surprise that some bacterial pathogens of humans and other mammals not only came from ancestors that attacked amoebas but often retained that ability over evolutionary time. These new and exciting results tell the detailed story of how a bacterium can exploit the social cycle of an amoeba and completely change the virulence genes it deploys according to whether it is attacking a hot mammal or a chilly amoeba. This example is likely to be only the first of many careful studies that reveal exactly how bacteria pull off these tricks.