Heat shock protein 60 sequence comparisons: duplications, lateral transfer, and mitochondrial evolution

Abstract

Heat shock proteins 60 (GroEL) are highly expressed essential proteins in eubacterial genomes and in eukaryotic organelles. These chaperone proteins have been advanced as propitious marker sequences for tracing the evolution of mitochondrial (Mt) genomes. Similarities among HSP60 sequences based on significant segment pair alignment calculations are used to deduce associations of sequences taking into account GroEL functional/structural domain differences and to relate HSP60 duplications pervasive in alpha-proteobacterial lineages to the dynamics of lateral transfer and plasmid integration. Multiple alignments with consensuses are determined for 10 natural groups. The group consensuses sharpen the similarity contrasts among individual sequences. In particular, the Mt group matches best with the classical alpha-proteobacteria and closely with Rickettsia but significantly worse with the rickettsial groups Ehrlichia and Orientia. However, across broad protein sequence comparisons, there appears to be no consistent prokaryote whose protein sequences align best with animal Mt genomes. There are plausible scenarios indicating that the nuclear-encoded HSP60 (and HSP70) sequences functioning in Mt are results of lateral transfer and are probably derived from an alpha-proteobacterium. This hypothesis relates to the plethora of duplicated HSP60 sequences among the classical alpha-proteobacteria contrasted with no duplications of HSP60 among other clades of proteobacterial genomes. Evolutionary relations are confounded by differential selection pressures, convergence, variable mutational rates, site variability, and lateral gene transfer.

Figure 1

SSPA similarities of bacterial and organellar HSP60 sequences.

Figure 2

SSPA Similarities between eubacterial and mitochondrial sequences are indicated for different protein families. Abr, Azospirillum brasilense; Aca, Acantamoeba castellanii; Ama, Allomyces macrogynus (Chytridiomycota); Ath, Arabidopsis thaliana; Bca, Bacillus coldotenax; Bsu, Bacillus subtilis; Cab, Clostridium acetobutylicum; Ccr, Chondrus crispus (Rhodophyta); Cel, Caenorhabditis elegans; Cma, Cucurbita maxima (pumpkin); Cre, Chlamydomonas reinhardtii; Dme, Drosophila melanogaster; Eco, Escherichia coli; Gga, Gallus gallus; Hum, human; Lta, Leishmania tarentolae; Mmu, mouse; Mpo, Marchantia polymorpha (liverwort); Ncr, Neurospora crassa; PARDE, Paracoccus denitrificans, Pfa, Plasmodium falciparum; Pwi, Prototheca wickerhamii (Chlorophyta); Ram, Reclinomonas americana; Rca, RHOCA, Rhodobacter capsulatus; Rme, Rhizobium meliloti; Rpr, Rickettsia prowazekii; Rsp, Rhodobacter sphaeroides; Sau, Streptomyces aureofaciens; Sce, Saccharomyces cerevisiae; Smu, Streptococcus mutans; Zma, maize. ¹α, Bradyrhizobium japonicum, Rhodobacter leguminosarum, R. sphaeroides; Nem, nematodes Ascaris suum (pig roundworm) and C. elegans; Fun, fungi Emericella nidulans, N. crassa, S. pombe, and S. cerevisiae; Pla, plants A. thaliana and maize; Kpl, kinetoplastida L. terentolae and Trypanosoma brucei brucei. ²α, P. denitrificans and R. sphaeroides; Nem, A. suum and C. elegans; Fun, N. crassa, S. cerevisiae, and S. pombe; Pla, plants D. carota (carrot) and maize. ³Mam, human and mouse; Nem, A. suum and C. elegans; Fun, N. crassa, S. pombe and Schizophyllum commune. ⁴Pla, A. thaliana and liverwort. ⁵Pla, A. thaliana and wheat. ⁶α, Rhodospirillum rubrum and R. capsulatus. ⁷Fun, Candida glabrata and S. cerevisiae. ⁸α, R. sphaeroides, R. capsulatus, and R. rubrum; Ver, vertebrates human, mouse, and chick; Fun, N. crassa and S. cerevisiae. ⁹α, R. meliloti and C. crescentus. ¹⁰γ, H. influenzae, E. coli, and Pseudomonas putida; Gr(−), Gram(−) BORBU, CHLTR, HELPY, TREPA, and SYNY3; Gr(+), Gram(+) BACSU and S. aureofaciens.