Extracellular Vesicles Could Carry an Evolutionary Footprint in Interkingdom Communication

Abstract

Extracellular vesicles (EVs) are minute particles secreted by the cells of living organisms. Although the functional role of EVs is not yet clear, recent work has highlighted their role in intercellular communication. Here, we expand on this view by suggesting that EVs can also mediate communication among interacting organisms such as hosts, pathogens and vectors. This inter-kingdom communication via EVs is likely to have important evolutionary consequences ranging from adaptation of parasites to specialized niches in the host, to host resistance and evolution and maintenance of parasite virulence and transmissibility. A potential system to explore these consequences is the interaction among the human host, the mosquito vector and Plasmodium parasite involved in the malaria disease. Indeed, recent studies have found that EVs derived from Plasmodium infected red blood cells in humans are likely mediating the parasite's transition from the asexual to sexual stage, which might facilitate transmission to the mosquito vector. However, more work is needed to establish the adaptive consequences of this EV signaling among different taxa. We suggest that an integrative molecular approach, including a comparative phylogenetic analysis of the molecules (e.g., proteins and nucleic acids) derived from the EVs of interacting organisms (and their closely-related species) in the malaria system will prove useful for understanding interkingdom communication. Such analyses will also shed light on the evolution and persistence of host, parasite and vector interactions, with implications for the control of vector borne infectious diseases.

Extracellular Vesicles in Fungi: Past, Present, and Future Perspectives

“…Despite the already mentioned open questions (Margolis and Sadovsky, 2019 ; Raposo and Stahl, 2019 ), substantial progress has been made to elevate EVs to the position of important mediators of intercellular and interkingdom communication processes, given their ability to transfer bioactive components (Maas et al, 2017 ; van Niel et al, 2018 ; Cai et al, 2019 ; Mathieu et al, 2019 ; Correa et al, 2020 ) and surmount biological barriers, including the blood-brain barrier (BBB) (Alvarez-Erviti et al, 2011 ).…”

Harnessing the Neural Stem Cell Secretome for Regenerative Neuroimmunology

“…The release of biological signals within phospholipid-bound membranes could have originated as a method of eliminating damaged cellular components, and subsequently, may have provided a warning to local and distant cells acting as a primitive immune system (van Niel et al, 2018;Margolis and Sadovsky, 2019;Correa et al, 2020). EVs are now known to be critical mediators of intercellular communication and even act on the immune system and immune cells (Robbins and Morelli, 2014;Isola and Chen, 2017).…”

Ancient Evolutionary Origin and Properties of Universally Produced Natural Exosomes Contribute to Their Therapeutic Superiority Compared to Artificial Nanoparticles

“…These ideas emphasize the potential long biologic evolution of exosomes over billions of years of Darwinian experimentation via the natural selection of optimal properties to achieve current day physiological nanovesicle exosomes [ 188 , 189 ]. Here, this is compared to the misguided industrial efforts of some current investigators who engineer artificial therapeutic nanovesicles for human use that, compared to EV-like exosomes, are deficient in many essential biologic properties that are proposed to have been generated via progressive steps in evolution of such EVs over billions of years [ 188 , 189 , 190 ].…”