Chimeric Protein Complexes in Hybrid Species Generate Novel Phenotypes

Abstract

Hybridization between species is an important mechanism for the origin of novel lineages and adaptation to new environments. Increased allelic variation and modification of the transcriptional network are the two recognized forces currently deemed to be responsible for the phenotypic properties seen in hybrids. However, since the majority of the biological functions in a cell are carried out by protein complexes, inter-specific protein assemblies therefore represent another important source of natural variation upon which evolutionary forces can act. Here we studied the composition of six protein complexes in two different Saccharomyces “sensu stricto” hybrids, to understand whether chimeric interactions can be freely formed in the cell in spite of species-specific co-evolutionary forces, and whether the different types of complexes cause a change in hybrid fitness. The protein assemblies were isolated from the hybrids via affinity chromatography and identified via mass spectrometry. We found evidence of spontaneous chimericity for four of the six protein assemblies tested and we showed that different types of complexes can cause a variety of phenotypes in selected environments. In the case of TRP2/TRP3 complex, the effect of such chimeric formation resulted in the fitness advantage of the hybrid in an environment lacking tryptophan, while only one type of parental combination of the MBF complex allowed the hybrid to grow under respiratory conditions. These phenotypes were dependent on both genetic and environmental backgrounds. This study provides empirical evidence that chimeric protein complexes can freely assemble in cells and reveals a new mechanism to generate phenotypic novelty and plasticity in hybrids to complement the genomic innovation resulting from gene duplication. The ability to exchange orthologous members has also important implications for the adaptation and subsequent genome evolution of the hybrids in terms of pattern of gene loss.

Author Summary

The Saccharomyces cerevisiae “sensu stricto” group represent an excellent example of closely related species which can readily hybridise to occupy new ecological niches. Hybrids harbour the DNA of both parents and can display diverse pattern of gene expression. Less is known about the protein interactions that occur in hybrids, where two diverged proteome co-exist and are responsible for the correct execution of the biological function. In fact, hybrids could potentially form different chimeric variants of the same protein complex by using all the different combinations of parental alleles available. Chimeric interactions are expected to be sub-optimal and therefore discouraged since the members forming the protein complex are from different parents and have a different evolutionary history. Interestingly, here, we show experimentally that chimeric protein assemblies are spontaneously established in different yeast hybrids, and that such chimericity produces different phenotypic variants displaying loss or gain of fitness according to their genetic background and to the environment that they are exposed. These findings imply that the formation of chimeric complexes offers a new source of natural variation, widens the adaptation potential of the hybrids towards new nutritional contexts, and may influence genome evolution through selective retention of optimal alleles.