Biological Functions of Prokaryotic Amyloids in Interspecies Interactions: Facts and Assumptions

Abstract

Amyloids are fibrillar protein aggregates with an ordered spatial structure called “cross-β”. While some amyloids are associated with development of approximately 50 incurable diseases of humans and animals, the others perform various crucial physiological functions. The greatest diversity of amyloids functions is identified within prokaryotic species where they, being the components of the biofilm matrix, function as adhesins, regulate the activity of toxins and virulence factors, and compose extracellular protein layers. Amyloid state is widely used by different pathogenic bacterial species in their interactions with eukaryotic organisms. These amyloids, being functional for bacteria that produce them, are associated with various bacterial infections in humans and animals. Thus, the repertoire of the disease-associated amyloids includes not only dozens of pathological amyloids of mammalian origin but also numerous microbial amyloids. Although the ability of symbiotic microorganisms to produce amyloids has recently been demonstrated, functional roles of prokaryotic amyloids in host–symbiont interactions as well as in the interspecies interactions within the prokaryotic communities remain poorly studied. Here, we summarize the current findings in the field of prokaryotic amyloids, classify different interspecies interactions where these amyloids are involved, and hypothesize about their real occurrence in nature as well as their roles in pathogenesis and symbiosis.

Current Understanding of the Structure, Stability and Dynamic Properties of Amyloid Fibrils

“…It has become increasingly clear that amyloid structures are not only found in aberrant and disease-related aggregates, but also in functional protein assemblies referred to as “functional amyloids” [ 7 ]. Functional amyloids are mainly produced by prokaryotes [ 6 , 55 ] and some of them are produced by higher eukaryotes [ 56 ]. It is currently understood that functional amyloids serve diverse purposes, and some of them act as biofilm matrix proteins playing a scaffolding role in microorganisms [ 6 , 55 ].…”

“…Functional amyloids are mainly produced by prokaryotes [ 6 , 55 ] and some of them are produced by higher eukaryotes [ 56 ]. It is currently understood that functional amyloids serve diverse purposes, and some of them act as biofilm matrix proteins playing a scaffolding role in microorganisms [ 6 , 55 ]. In filamentous fungi, amyloid fibrils organize an amphipathic monolayer by assembling laterally on the surface of a hydrophobic/hydrophilic interface, thus reversing wettability, as seen in water-repellent spore coats [ 57 ].…”

“…In filamentous fungi, amyloid fibrils organize an amphipathic monolayer by assembling laterally on the surface of a hydrophobic/hydrophilic interface, thus reversing wettability, as seen in water-repellent spore coats [ 57 ]. There are also functional amyloids playing other roles such as virulence, protection against degradation and adhesion [ 55 , 58 ], as well as in the more complicated regulatory functions in the transcription, heterokaryon incompatibility, and long-term memory, etc. of eukaryotes, as have also been reported [ 56 ].…”

“…Curli is one of the functional amyloids serving as a scaffold in bacterial biofilms [ 6 , 55 ]. Since the discovery of the amyloid-like structure in curli produced by Escherichia coli by Chapman et al [ 59 ], the biosynthesis mechanism of E. coli curli has attracted attention as an important example where the location and timing of formation are finely controlled [ 60 ].…”

Amyloids: The History of Toxicity and Functionality

“…Amyloids have also an RNA-modulating ability and play a role in transcription, translation, storage and degradation of RNA [ 173 ]. It has been shown that some motifs in prions of fungi and humans can be functionally related and be a model of amyloid signaling mechanisms from fungi to mammals [ 174 , 175 ]. Prokaryotic cells can also use such properties [ 8 ].…”