The trojan horse relationship between amoebae and bacteria
Ronnie Mooney, Elisa Giammarini, Jackie Parry and Fiona L. Henriquez
P redator–prey interactions are amongst the most significant driving forces of evolution throughout all kingdoms of life. Evermore complex strategies for predation or evasion continue to be uncovered, and perhaps the interactions with the biggest impact on life occur at the microbial level. The free-living amoebae (FLA) present an interesting group of protists that obtain much of their nutrients through the predation of other microbial species, in particular bacteria. The FLA are essential in the regulation of bacterial communities within soil and aquatic ecosystems, engulfing and feeding on captured bacteria in a process known as phagocytosis (Figure 1). Generally, the predation of bacteria by protists is considered beneficial, and as much as 60% of bacterial species are regulated by amoebic phagocytosis, promoting ecosystem health and diversity. The efficiency whereby the FLA and other predatory protists can reduce bacterial populations has been exploited in water treatment processes to improve water quality and reduce the presence of bacterial pathogens. What we often fail to consider, however, is the impact of these interactions on human health. As protists have evolved strategies to predate bacteria, bacteria have evolved strategies to evade protists. While bacterial predation is largely beneficial, generations of predation by FLA on bacteria have given rise to sophisticated strategies that allow bacteria to evade the phagocytic mechanisms employed by the FLA. The evasion strategies are complex and many; while some allow the avoidance of detection by the amoebae, others permit intracellular survival. Herein, we focus on those bacteria capable of surviving intracellularly within FLA (amoeba- resistant bacteria) and discuss how this ongoing evolutionary arms race may have far-reaching implications on human health, driving antimicrobial resistance, complicating detection of pathogens and influencing disease outcomes.
Our reliance on effective antimicrobials might prove to have severe long-term consequences unless we can formulate effective mitigation strategies to slow the spread of AMR in the environment. To do this, we need to understand the factors that drive the evolution of AMR. Industrial pollution, pharmaceutical manufacturing, aquaculture and agriculture are commonly cited factors influencing the presence of AMR within the environment, and rightly so, yet the wider interactions between different micro-organism groups are less considered. Horizontal gene transfer (HGT) is the transfer of genetic material between two micro-organisms. In bacteria, this transfer of genes promotes genetic diversity and is a major contributor to the spread of AMR genes throughout bacterial populations. Briefly, genes that confer AMR can be passed between bacteria, occurring more frequently when the organisms are in close contact. Organisms that possess these genes gain a selection advantage when exposed to specific antimicrobials within the environment, which may prompt further spread of the gene. Interestingly, the conditions that promote gene transfer can be amplified during intracellular survival within amoebae. The intracellular environment of the amoebae has been described as a ‘genetic melting pot’, an environment that serves to fast track the transfer of genetic material between engulfed organisms. The ingestion of multiple phagocyte-resistant bacteria results in a highly dense population of cells within the amoebae, increasing the likelihood that gene transfer events might take place. Additionally, intracellular survival within the amoebae might also serve to reduce exposure to environmental antimicrobials to sub-inhibitory levels, ultimately selecting for increasingly resistant bacteria. Recently, genomic analysis of intracellular bacteria within amoebae revealed that HGT events were ongoing within the amoebae and identified transferred genes important in antibiotic resistance, stress tolerance, amoeba– bacteria interactions and virulence. Interestingly, the gene transfer events are not uniquely between bacteria, with studies demonstrating the acquisition by amoebae of genes from bacterial symbionts that might aid in reducing oxidative stress.
The genetic melting pot – amoebae, bacteria and antimicrobial resistance
Antimicrobial resistance (AMR) is undoubtedly one of the most significant emerging threats facing human health.
76 Microbiology Today October 2022 | microbiologysociety.org
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