Phagocyte chase behaviours: discrimination between Gram-negative and Gram-positive bacteria by amoebae

Abstract

Phagocytes are cells that pursue, engulf and kill bacteria. They include macrophages and neutrophils of the mammalian immune system, as well as free-living amoebae that hunt and engulf bacteria for food. Phagocytosis can result in diverse outcomes, ranging from sustenance to infection and colonization by either pathogens or beneficial symbionts-and thus, discrimination may be necessary to seek out good bacteria while avoiding bad ones.Here we tested whether the soil amoeba Dictyostelium discoideum can discriminate among different types of bacteria using behavioural assays where amoebae were presented with paired choices of different bacteria. We observed variation in the extent to which the amoebae pursued different types of bacteria, as well as preferential migration towards Gram-negative compared with Gram-positive bacteria. Response profiles were similar for amoebae that originated from different geographical locations, suggesting that chase preference is conserved across much of the species range. While prior work has demonstrated that bacteria use chemotaxis to seek out amoebae they colonize, our work suggests that the opposite also occursamoebae can preferentially direct themselves to particular bacteria in the environment. Preferential sensing and response may help to explain why some amoeba-bacteria associations are more common in nature than others.

Characterization of the bacterial microbiomes of social amoebae and exploration of the roles of host and environment on microbiome composition

“…Brock et al (2018) found that 81% of culturable symbionts of D. discoideum were edible. The ability of social amoebae to preferentially chemotax toward gram-negative bacteria (Rashidi and Ostrowski, 2019) may also increase the likelihood of potential gram-negative bacterial symbionts being passively transmitted from the environment.…”

A dormant amoeba species can selectively sense and predate on different soil bacteria

“…discoideum had different gene expression profiles when exposed to different bacteria (Benghezal et al., 2006; Lamrabet et al., 2020; Nasser et al., 2013). They were also more attracted to Gram‐negative bacteria in a chemotaxis assay (Rashidi & Ostrowski, 2019). However, it is not clear whether such food preference is determined by bacterial nutrition (greater production of amoeba spores after feeding on a given amount of bacteria).…”

“…A previous study found that D . discoideum prefers Gram‐negative bacteria in a chemotaxis assay (Rashidi & Ostrowski, 2019). This study further shows that D .…”

“…We used four different bacterial densities to test the inhibition effect of 14 different bacterial species on amoeba predation and growth. We focused on species‐level variations, as well as Gram‐stain type and bacterial motility because existing evidence suggests that cell wall types and energy expenditure may impact protist–bacterium interactions (Matz & Jurgens, 2005; Nasser et al., 2013; Rashidi & Ostrowski, 2019).…”

The past, present and future of Dictyostelium as a model system

“…Genetic studies involving knockout mutants, unbiased mutational screens, genome-wide transcriptional changes and proteomic analysis during phagocytosis, macropinocytosis or infection have produced a large wealth of data, which have been the subject of several reviews in the last years (Bozzaro and Eichinger, 2011;Dunn et al, 2018;Cardenal-Muñoz et al, 2018;Swart et al, 2018). Among more recent data not yet covered by reviews, it is worth mentioning: (I) evidence that Dictyostelium cells are highly sensitive to bacterial chemoattractants, but phagocytosis per se is independent of chemoreceptor sensing (Meena and Kimmel, 2017); (II) in apparent contrast to this, the characterization of the G protein-coupled, folic acid receptor fAR1, which recognizes the saccharide core of LPS and stimulates gram-negative bacterial phagocytosis, providing a plausible mechanism for the involvement of G proteins in phagocytosis ; discrepancy between both results may be due to the different phagocytosis assays used; (III) evidence that Dictyostelium discriminates between Gram-(-) and Gram-(+) bacteria, migrating preferentially toward Gram-(-) bacteria (Rashidi and Ostrowski, 2019), and that their growth on Gram-(-) or Gram-(+) bacteria elicit different transcriptomic profiles, with some genes essential for growth (Nasser et al, 2013); ((IV) the identification of PIKFyve/FAB1 in controlling acidification of phagosomes (Buckley et al, 2019), thus extending previous studies on the role of phosphoinositides in phagocytosis, macropinocytosis and resistance to pathogens (Swart et al, 2018;Hoeller et al, 2013;Peracino et al, 2010; (V) Similarly, it has been shown that the RasGAP IqgC is a negative regulator of macropinocytosis and large particle phagocytosis (Marinović et al, 2019), strengthening the role of Ras signalling in these processes Junemann et al, 2016;Bolourani et al, 2010; (VI) While bacterial phagocytosis is essential for growth, it has also been shown that during slug stage, cells maintain as endosymbionts bacteria that have been coated with the secreted lectin discoidin I, and that could possibly be used later as a food source (Dinh et al, 2018).…”