Yeast proteins do not practice social distancing as species hybridize

Abstract

With the current COVID-19 pandemic, we all realized how important interactions are. Interactions are everywhere. At the cellular level, protein interactions play a key role and their ensemble, also called interactome, is often referred as the basic building blocks of life. Given its importance, the maintenance of the integrity of the interactome is a real challenge in the cell. Many events during evolution can disrupt interactomes and potentially result in different characteristics for the organisms. However, the molecular underpinnings of changes in interactions at the cellular level are still largely unexplored. Among the perturbations, hybridization puts in contact two different interactomes, which may lead to many changes in the protein interaction network of the hybrid, including gains and losses of interactions. We recently investigated the fate of the interactomes after hybridization between yeast species using a comparative proteomics approach. A large-scale conservation of the interactions was observed in hybrids, but we also noticed the presence of proteostasis-related changes. This suggests that, despite a general robustness, small differences may accumulate in hybrids and perturb their protein physiology. Here, we summarize our work with a broader perspective on the importance of interactions.

Keywords: Hybridization; Interactome; Protein–protein interaction; Yeast.

Fig. 1

Interactions between species can disrupt the interactome. a Viral infections (top panel) lead to contact between proteins of the host and the virus. Interactions between viral and host proteins (thick red lines) will disrupt the host interactome (red dotted lines) and therefore cellular processes. b In bacterial infections (center), the host interactome is disrupted by effector proteins from the bacteria (rather than by the entire interactome of the bacteria) (thick red line). These effectors can also modify the interactome of the host (red dotted lines). c In the case of hybridization between two distinct species (bottom panel), there is an initial mix of the two parental interactomes (step 1). After hybridization (step 2), the interactome of the hybrid will be composed of inter-species interactions also called chimeric interactions (red lines) and intra-species interactions also called parental interactions (black lines). Some interactions will have been disrupted (red dotted lines), while others will appear (thick red lines). Adapted from (Diss et al. 2013)

Fig. 2

SEC–PCP–SILAC enables comparing the interactomes of a parental and b hybrid yeast species. This method allows obtaining protein elution profiles that are subsequently used to infer protein interactions and protein complexes. The principle of the analysis is that two proteins (P1 and P2) that interact will tend to have similar elution profiles over time. a Interaction between P1 and P2 is detected in both parents. b In our study, we demonstrated that after hybridization, there is a mix of the two parental interactomes: P1 of parent two interacts with P2 of parent one and the reverse, P1 of parent one interacts with P2 of parent two. The interactome of the hybrid is, thus, mostly composed of inter-species interactions (chimeric interactions)