Reduced bonobo MHC class I diversity predicts a reduced viral peptide binding ability compared to chimpanzees

Vincent Maibach,Linda Vigilant

doi:10.1186/s12862-019-1352-0

Abstract

BackgroundThe highly polymorphic genes of the major histocompatibility complex (MHC) class I are involved in defense against viruses and other intracellular pathogens. Although several studies found reduced MHC class I diversity in bonobos in comparison to the closely related chimpanzee, it is unclear if this lower diversity also influences the functional ability of MHC class I molecules in bonobos. Here, we use a bioinformatic approach to analyze the viral peptide binding ability of all published bonobo MHC class I molecules (n = 58) in comparison to all published chimpanzee MHC class I molecules (n = 161) for the class I loci A, B, C and A-like.ResultsWe examined the peptide binding ability of all 219 different MHC class I molecules to 5,788,712 peptides derived from 1432 different primate viruses and analyzed the percentage of bound peptides and the overlap of the peptide binding repertoires of the two species. We conducted multiple levels of analysis on the “species”-, “population”- and “individual”-level to account for the characterization of MHC variation in a larger number of chimpanzees and their broader geographic distribution. We found a lower percentage of bound peptides in bonobos at the B locus in the “population”-level comparison and at the B and C loci in the “individual”-level comparison. Furthermore, we found evidence of a limited peptide binding repertoire in bonobos by tree-based visualization of functional clustering of MHC molecules, as well as an analysis of peptides bound by both species.ConclusionOur results suggest a reduced MHC class I viral peptide binding ability at the B and C loci in bonobos compared to chimpanzees. The effects of this finding on the immune defense against viruses in wild living bonobos are unclear. However, special caution is needed to prevent introduction and spread of new viruses to bonobos, as their defensive ability to cope with new viruses could be limited compared to chimpanzees.

Highlights

The highly polymorphic genes of the major histocompatibility complex (MHC) class I are involved in defense against viruses and other intracellular pathogens
In total we bioinformatically compared 219 different MHC molecules to a set of 5,788,712 nine amino acid long viral peptides derived from a dataset of 1432 viruses
We found no correlation between the number of occurrences of a peptide in our dataset and the number of MHC molecules which bound those peptides, suggesting that even some common peptides sequences may not be bound by multiple MHC molecules (Pearson’s product-moment correlation, t = − 2.4937, df = 108,740, p = 0.01264, r = − 0.0076)

Summary

Introduction

The highly polymorphic genes of the major histocompatibility complex (MHC) class I are involved in defense against viruses and other intracellular pathogens. We use a bioinformatic approach to analyze the viral peptide binding ability of all published bonobo MHC class I molecules (n = 58) in comparison to all published chimpanzee MHC class I molecules (n = 161) for the class I loci A, B, C and A-like. The most diverse genes found in higher vertebrates constitute the major histocompatibility complex (MHC). These genes underpin the mammalian adaptive immune system by coding for molecules presenting peptides to immunocompetent cells [1,2,3]. Bonobos exist in a single geographic range comparable in size to the range of a single chimpanzee subspecies and have limited genetic substructure [18, 19]

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