Sequence-based analysis of thermal adaptation and protein energy landscapes in an invasive blue mussel (Mytilus galloprovincialis).

5 years ago

Sequence-based analysis of thermal adaptation and protein energy landscapes in an invasive blue mussel (Mytilus galloprovincialis).

Saarman, Pogson, Kober, Simison

Adaptive responses to thermal stress in poikilotherms plays an important role in determining competitive ability and species distributions. Amino acid substitutions that affect protein stability and modify the thermal optima of orthologous proteins may be particularly important in this context. Here, we examine a set of 2,770 protein-coding genes to determine if proteins in a highly invasive heat tolerant blue mussel (Mytilus galloprovincialis) contain signals of adaptive increases in protein stability relative to orthologs in a more cold-tolerant M. trossulus. Such thermal adaptations might help to explain, mechanistically, the success with which the invasive M. galloprovincialis has displaced native species in contact zones in the eastern (California) and western (Japan) Pacific. We tested for stabilizing amino acid substitutions in warm tolerant M. galloprovincialis relative to cold tolerant M. trossulus with a generalized linear model that compares in silico estimates of recent changes in protein stability among closely related congeners. Fixed substitutions in M. galloprovincialis were 3,180.0 calories per mol per substitution more stabilizing at genes with both elevated dN/dS ratios and transcriptional responses to heat stress, and 705.8 calories per mol per substitution more stabilizing across all 2,770 loci investigated. Amino acid substitutions concentrated in a small number of genes were more stabilizing in M. galloprovincialis compared to cold tolerant M. trossulus. We also tested for, but did not find, enrichment of a priori GO terms in genes with elevated dN/dS ratios in M. galloprovincialis. This might indicate that selection for thermodynamic stability is generic across all lineages, and suggests that the high ΔΔGstab that we observe in M. galloprovincialis is driven by selection for extra stabilizing substitutions rather than higher incidence of selection in a greater number of genes in this lineage. Nonetheless, our finding of more stabilizing amino acid changes in the warm adapted lineage relative to cold adapted congeners is important because it suggests that adaption for thermal stability in M. galloprovincialis has contributed to this species' superior tolerance to heat stress, and that pairing tests for positive selection and tests for transcriptional response to heat stress can identify candidates of protein stability adaptation.

Publisher URL: http://doi.org/10.1093/gbe/evx190

DOI: 10.1093/gbe/evx190