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Substrate adaptabilities of Thermotogae mannan binding proteins as a function of their evolutionary histories

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Abstract

The Thermotogae possess a large number of ATP-binding cassette (ABC) transporters, including two mannan binding proteins, ManD and CelE (previously called ManE). We show that a gene encoding an ancestor of these was acquired by the Thermotogae from the archaea followed by gene duplication. To address the functional evolution of these proteins as a consequence of their evolutionary histories, we measured the binding affinities of ManD and CelE orthologs from representative Thermotogae. Both proteins bind cellobiose, cellotriose, cellotetraose, β-1,4-mannotriose, and β-1,4-mannotetraose. The CelE orthologs additionally bind β-1,4-mannobiose, laminaribiose, laminaritriose and sophorose while the ManD orthologs additionally only weakly bind β-1,4-mannobiose. The CelE orthologs have higher unfolding temperatures than the ManD orthologs. An examination of codon sites under positive selection revealed that many of these encode residues located near or in the binding site, suggesting that the proteins experienced selective pressures in regions that might have changed their functions. The gene arrangement, phylogeny, binding properties, and putative regulatory networks suggest that the ancestral mannan binding protein was a CelE ortholog which gave rise to the ManD orthologs. This study provides a window on how one class of proteins adapted to new functions and temperatures to fit the physiologies of their new hosts.

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Acknowledgments

Access to the spectrofluorometer was graciously provided by Dr. Carol Teschke. We thank Drs. J. Peter Gogarten and Pascal Lapierre for discussions involving the phylogenetic and branched site model analyses. This work was supported by the NASA Astrobiology program (NNX08AQ10G), the U.S. Department of Energy Office of Biological and Environmental Research (DE-PS02-08ER08-12), and the National Science Foundation Assembling the Tree of Life program (DEB0830024).

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  1. Nathalie Boucher

    Present address: New York State Department of Health, Wadsworth Center, Albany, NY, 12201, USA

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  1. Department of Molecular and Cell Biology, University of Connecticut, Unit 3125, 91 N. Eagleville Rd., Storrs, CT, 06269-3125, USA

    Nathalie Boucher & Kenneth M. Noll

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  1. Nathalie Boucher
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Correspondence to Kenneth M. Noll.

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Communicated by F. Robb.

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792_2016_866_MOESM1_ESM.pdf

Figure S1. ClustalX sequence alignment of TmarCelE and TmarManD. Figure modified from (Ghimire-Rijal et al. 2014). Amino acid numbering includes the signal peptides which were not included in the alignment. Residues forming the metal binding site are highlighted in gray. The laminaripentaose specificity-determining loop is in boldface. Amino acids that interact with the six sugar rings are denoted with colored type as follows: first (red), second (orange), third (green), fourth (cyan), fifth (purple), and sixth (magenta). Residues that form hydrogen bonds to the sugar are underlined. When a residue interacts with more than one sugar ring, only the first sugar ring color is shown. Residues under positive selection are highlighted in green. Sequence comparisons are indicated by (*), identical amino acids between both sequences; (:), strongly conserved substitutions; and (.) are weakly conserved substitutions. (PDF 47 kb)

792_2016_866_MOESM2_ESM.pdf

Figure S2. Codon sites under positive selection mapped onto the CelETmar (A and B) and ManDTmar (C and D) crystal structures [pdb: 4pfw (ManD) and 4pfy (CelE)]. The active sites are magnified in B and D. The residues encoded by the codons under positive selection (class 2a) are highlighted as follows: residues 514 (ManD and CelE) and 519 (CelE) in the binding pocket are red, other residues in the binding pocket are orange, and those outside the binding pocket are blue. The β-1,4-mannohexaose is green with the sixth ring at the bottom in each figure. (PDF 481 kb)

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Boucher, N., Noll, K.M. Substrate adaptabilities of Thermotogae mannan binding proteins as a function of their evolutionary histories. Extremophiles 20, 771–783 (2016). https://doi.org/10.1007/s00792-016-0866-2

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