AlphaFold2-guided description of CoBaHMA, a novel family of bacterial domains within the heavy-metal-associated superfamily.
ABC transporter
AlphaFold2
CoBaHMA
P1B-ATPase
PAP2
biomineralization
functional annotation
graph clustering
heavy-metal-associated
modular organization
sequence similarity search
Journal
Proteins
ISSN: 1097-0134
Titre abrégé: Proteins
Pays: United States
ID NLM: 8700181
Informations de publication
Date de publication:
22 Jan 2024
22 Jan 2024
Historique:
revised:
22
12
2023
received:
28
09
2023
accepted:
01
01
2024
medline:
23
1
2024
pubmed:
23
1
2024
entrez:
23
1
2024
Statut:
aheadofprint
Résumé
Three-dimensional (3D) structure information, now available at the proteome scale, may facilitate the detection of remote evolutionary relationships in protein superfamilies. Here, we illustrate this with the identification of a novel family of protein domains related to the ferredoxin-like superfold, by combining (i) transitive sequence similarity searches, (ii) clustering approaches, and (iii) the use of AlphaFold2 3D structure models. Domains of this family were initially identified in relation with the intracellular biomineralization of calcium carbonates by Cyanobacteria. They are part of the large heavy-metal-associated (HMA) superfamily, departing from the latter by specific sequence and structural features. In particular, most of them share conserved basic amino acids (hence their name CoBaHMA for Conserved Basic residues HMA), forming a positively charged surface, which is likely to interact with anionic partners. CoBaHMA domains are found in diverse modular organizations in bacteria, existing in the form of monodomain proteins or as part of larger proteins, some of which are membrane proteins involved in transport or lipid metabolism. This suggests that the CoBaHMA domains may exert a regulatory function, involving interactions with anionic lipids. This hypothesis might have a particular resonance in the context of the compartmentalization observed for cyanobacterial intracellular calcium carbonates.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Agence Nationale de la Recherche
ID : ANR-19-CE44-0017-01
Organisme : Agence Nationale de la Recherche
ID : ANR-19-CE01-0005
Informations de copyright
© 2024 The Authors. Proteins: Structure, Function, and Bioinformatics published by Wiley Periodicals LLC.
Références
Orengo CA, Jones DT, Thornton JM. Protein superfamilies and domain superfolds. Nature. 1994;372(6507):631-634.
Chitturi B, Shi S, Kinch LN, Grishin NV. Compact structure patterns in proteins. J Mol Biol. 2016;428(21):4392-4412.
Kolodny R. Searching protein space for ancient sub-domain segments. Curr Opin Struct Biol. 2021;68:105-112.
Chandonia JM, Guan L, Lin S, Yu C, Fox NK, Brenner SE. SCOPe: improvements to the structural classification of proteins-extended database to facilitate variant interpretation and machine learning. Nucleic Acids Res. 2022;50(D1):D553-D559.
Caetano-Anollés G, Caetano-Anollés D. An evolutionarily structured universe of protein architecture. Genome Res. 2003;13(7):1563-1571.
Thornton JM, Orengo CA, Todd AE, Pearl FM. Protein folds, functions and evolution. J Mol Biol. 1999;293(2):333-342.
Grishin NV. Fold change in evolution of protein structures. J Struct Biol. 2001;134(2-3):167-185.
Jung J, Lee B. Circularly permuted proteins in the protein structure database. Protein Sci. 2001;10(9):1881-1886.
Arnesano F, Banci L, Bertini I, et al. Metallochaperones and metal-transporting ATPases: a comparative analysis of sequences and structures. Genome Res. 2002;12(2):255-271.
Bull PC, Cox DW. Wilson disease and Menkes disease: new handles on heavy-metal transport. Trends Genet. 1994;10(7):246-252.
Palmgren MG, Nissen P. P-type ATPases. Annu Rev Biophys. 2011;40:243-266.
Benzerara K, Duprat E, Bitard-Feildel T, et al. A new gene family diagnostic for intracellular biomineralization of amorphous Ca carbonates by cyanobacteria. Genome Biol Evol. 2022;14(3):evac026.
Kim S, Chamberlain AK, Bowie JU. Membrane channel structure of Helicobacter pylori vacuolating toxin: role of multiple GXXXG motifs in cylindrical channels. Proc Natl Acad Sci USA. 2004;101(16):5988-5991.
Kim S, Jeon TJ, Oberai A, Yang D, Schmidt JJ, Bowie JU. Transmembrane glycine zippers: physiological and pathological roles in membrane proteins. Proc Natl Acad Sci USA. 2005;102(40):14278-14283.
De la Concepcion JC, Franceschetti M, Maqbool A, et al. Polymorphic residues in rice NLRs expand binding and response to effectors of the blast pathogen. Nat Plants. 2018;4(8):576-585.
Jiang D, Zhao Y, Fan J, et al. Atomic resolution structure of the E. coli YajR transporter YAM domain. Biochem Biophys Res Commun. 2014;450(2):929-935.
Jiang D, Zhao Y, Wang X, et al. Structure of the YajR transporter suggests a transport mechanism based on the conserved motif A. Proc Natl Acad Sci USA. 2013;110(36):14664-14669.
Faure G, Callebaut I. Identification of hidden relationships from the coupling of hydrophobic cluster analysis and domain architecture information. Bioinformatics. 2013;29(14):1726-1733.
Jin J, Xie X, Chen C, et al. Eukaryotic protein domains as functional units of cellular evolution. Sci Signal. 2009;2(98):ra76.
Vogel C, Bashton M, Kerrison ND, Chothia C, Teichmann SA. Structure, function and evolution of multidomain proteins. Curr Opin Struct Biol. 2004;14(2):208-216.
Jumper J, Evans R, Pritzel A, et al. Highly accurate protein structure prediction with AlphaFold. Nature. 2021;596(7873):583-589.
Varadi M, Anyango S, Deshpande M, et al. AlphaFold Protein Structure Database: massively expanding the structural coverage of protein-sequence space with high-accuracy models. Nucleic Acids Res. 2022;50(D1):D439-D444.
Mirdita M, von den Driesch L, Galiez C, Martin MJ, Söding J, Steinegger M. Uniclust databases of clustered and deeply annotated protein sequences and alignments. Nucleic Acids Res. 2017;45(D1):D170-d176.
Steinegger M, Meier M, Mirdita M, Vöhringer H, Haunsberger SJ, Söding J. HH-suite3 for fast remote homology detection and deep protein annotation. BMC Bioinformatics. 2019;20(1):473.
Kabsch W, Sander C. Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers. 1983;22(12):2577-2637.
Touw WG, Baakman C, Black J, et al. A series of PDB-related databanks for everyday needs. Nucleic Acids Res. 2015;43:D364-D368.
Rost B, Eyrich VA. EVA: large-scale analysis of secondary structure prediction. Proteins. 2001;suppl 5:192-199.
Ettema TJ, Huynen MA, de Vos WM, van der Oost J. TRASH: a novel metal-binding domain predicted to be involved in heavy-metal sensing, trafficking and resistance. Trends Biochem Sci. 2003;28(4):170-173.
UniProt: the universal protein knowledgebase in 2023. Nucleic Acids Res. 2023;51(D1):D523-d531.
Shen W, Ren H. TaxonKit: a practical and efficient NCBI taxonomy toolkit. J Genet Genomics. 2021;48(9):844-850.
Jones P, Binns D, Chang HY, et al. InterProScan 5: genome-scale protein function classification. Bioinformatics. 2014;30(9):1236-1240.
Blum M, Chang HY, Chuguransky S, et al. The InterPro protein families and domains database: 20 years on. Nucleic Acids Res. 2021;49(D1):D344-d354.
Manriquez-Sandoval E, Fried SD. DomainMapper: accurate domain structure annotation including those with non-contiguous topologies. Protein Sci. 2022;31(11):e4465.
Hallgren J, Tsirigos KD, Pedersen MD, et al. DeepTMHMM predicts alpha and beta transmembrane proteins using deep neural networks. bioRxiv 2022:2022.2004.2008.487609.
Bitard-Feildel T, Lamiable A, Mornon JP, Callebaut I. Order in disorder as observed by the “hydrophobic cluster analysis” of protein sequences. Proteomics. 2018;18(21-22):e1800054.
Callebaut I, Labesse G, Durand P, et al. Deciphering protein sequence information through hydrophobic cluster analysis (HCA): current status and perspectives. Cell Mol Life Sci. 1997;53(8):621-645.
Bruley A, Bitard-Feildel T, Callebaut I, Duprat E. A sequence-based foldability score combined with AlphaFold2 predictions to disentangle the protein order/disorder continuum. Proteins. 2023;91(4):466-484.
Bruley A, Mornon JP, Duprat E, Callebaut I. Digging into the 3D structure predictions of AlphaFold2 with low confidence: disorder and beyond. Biomolecules. 2022;12(10):1467.
Finn RD, Clements J, Eddy SR. HMMER web server: interactive sequence similarity searching. Nucleic Acids Res. 2011;39:W29-W37.
Larralde M, Zeller G. PyHMMER: a python library binding to HMMER for efficient sequence analysis. Bioinformatics. 2023;39(5):btad214.
Steinegger M, Söding J. MMseqs2 enables sensitive protein sequence searching for the analysis of massive data sets. Nat Biotechnol. 2017;35(11):1026-1028.
Gibbons TR, Mount SM, Cooper ED, Delwiche CF. Evaluation of BLAST-based edge-weighting metrics used for homology inference with the Markov Clustering algorithm. BMC Bioinformatics. 2015;16:218.
Hagberg A, Swart P, S Chult D. Exploring network structure, dynamics, and function using networkx. Conference: SCIPY 08; August 21. 2008 Pasadena, USA.
Blondel VD, Guillaume J-L, Lambiotte R, Lefebvre E. Fast unfolding of communities in large networks. J Stat Mech Theory Exp. 2008;2008(10):P10008.
Shannon P, Markiel A, Ozier O, et al. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 2003;13(11):2498-2504.
Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013;30(4):772-780.
Waterhouse AM, Procter JB, Martin DM, Clamp M, Barton GJ. Jalview version 2-a multiple sequence alignment editor and analysis workbench. Bioinformatics. 2009;25(9):1189-1191.
Crooks GE, Hon G, Chandonia JM, Brenner SE. WebLogo: a sequence logo generator. Genome Res. 2004;14(6):1188-1190.
Pettersen EF, Goddard TD, Huang CC, et al. UCSF ChimeraX: structure visualization for researchers, educators, and developers. Protein Sci. 2021;30(1):70-82.
Tunyasuvunakool K, Adler J, Wu Z, et al. Highly accurate protein structure prediction for the human proteome. Nature. 2021;596(7873):590-596.
van Kempen M, Kim SS, Tumescheit C, et al. Fast and accurate protein structure search with Foldseek. Nat Biotechnol. 2023. doi:10.1038/s41587-023-01773-0.
Robert X, Gouet P. Deciphering key features in protein structures with the new ENDscript server. Nucleic Acids Res. 2014;42:W320-W324.
Andersson M, Mattle D, Sitsel O, et al. Copper-transporting P-type ATPases use a unique ion-release pathway. Nat Struct Mol Biol. 2014;21(1):43-48.
Gourdon P, Liu XY, Skjørringe T, et al. Crystal structure of a copper-transporting PIB-type ATPase. Nature. 2011;475(7354):59-64.
Toyoshima C, Nakasako M, Nomura H, Ogawa H. Crystal structure of the calcium pump of sarcoplasmic reticulum at 2.6 A resolution. Nature. 2000;405(6787):647-655.
Smith AT, Smith KP, Rosenzweig AC. Diversity of the metal-transporting P1B-type ATPases. J Biol Inorg Chem. 2014;19(6):947-960.
Thomas C, Aller SG, Beis K, et al. Structural and functional diversity calls for a new classification of ABC transporters. FEBS Lett. 2020;594(23):3767-3775.
Leskelä S, Kontinen VP, Sarvas M. Molecular analysis of an operon in Bacillus subtilis encoding a novel ABC transporter with a role in exoprotein production, sporulation and competence. Microbiology. 1996;142(Pt 1):71-77.
Sigal YJ, McDermott MI, Morris AJ. Integral membrane lipid phosphatases/phosphotransferases: common structure and diverse functions. Biochem J. 2005;387(Pt 2):281-293.
Stukey J, Carman GM. Identification of a novel phosphatase sequence motif. Protein Sci. 1997;6(2):469-472.
Dillon DA, Wu WI, Riedel B, Wissing JB, Dowhan W, Carman GM. The Escherichia coli pgpB gene encodes for a diacylglycerol pyrophosphate phosphatase activity. J Biol Chem. 1996;271(48):30548-30553.
Zhao J, An J, Hwang D, et al. The lipid a 1-phosphatase, LpxE, functionally connects multiple layers of bacterial envelope biogenesis. MBio. 2019;10(3):e00886-19.
Miller DJ, Jerga A, Rock CO, White SW. Analysis of the Staphylococcus aureus DgkB structure reveals a common catalytic mechanism for the soluble diacylglycerol kinases. Structure. 2008;16(7):1036-1046.
Bakali MA, Nordlund P, Hallberg BM. Expression, purification, crystallization and preliminary diffraction studies of the mammalian DAG kinase homologue YegS from Escherichia coli. Acta Crystallogr Sect F Struct Biol Cryst Commun. 2006;62(Pt 3):295-297.
Borgstahl GE, Parge HE, Hickey MJ, Beyer WF Jr, Hallewell RA, Tainer JA. The structure of human mitochondrial manganese superoxide dismutase reveals a novel tetrameric interface of two 4-helix bundles. Cell. 1992;71(1):107-118.
Kleiger G, Grothe R, Mallick P, Eisenberg D. GXXXG and AXXXA: common alpha-helical interaction motifs in proteins, particularly in extremophiles. Biochemistry. 2002;41(19):5990-5997.
Beamer LJ, Carroll SF, Eisenberg D. Crystal structure of human BPI and two bound phospholipids at 2.4 angstrom resolution. Science. 1997;276(5320):1861-1864.
Kleiger G, Beamer LJ, Grothe R, Mallick P, Eisenberg D. The 1.7 a crystal structure of BPI: a study of how two dissimilar amino acid sequences can adopt the same fold. J Mol Biol. 2000;299(4):1019-1034.
Kopec KO, Alva V, Lupas AN. Bioinformatics of the TULIP domain superfamily. Biochem Soc Trans. 2011;39(4):1033-1038.
Koehler Leman J, Szczerbiak P, Renfrew PD, et al. Sequence-structure-function relationships in the microbial protein universe. Nat Commun. 2023;14(1):2351.
Salem GM, Hutchinson EG, Orengo CA, Thornton JM. Correlation of observed fold frequency with the occurrence of local structural motifs. J Mol Biol. 1999;287:969-981.
Alva V, Soding J, Lupas AN. A vocabulary of ancient peptides at the origin of folded proteins. eLife. 2015;4:e09410.
Jordan IK, Natale DA, Koonin EV, Galperin MY. Independent evolution of heavy metal-associated domains in copper chaperones and copper-transporting atpases. J Mol Evol. 2001;53(6):622-633.
Wang K, Sitsel O, Meloni G, et al. Structure and mechanism of Zn2+-transporting P-type ATPases. Nature. 2014;514(7523):518-522.
Mattle D, Sitsel O, Autzen HE, Meloni G, Gourdon P, Nissen P. On allosteric modulation of P-type Cu(+)-ATPases. J Mol Biol. 2013;425(13):2299-2308.
Biemans-Oldehinkel E, Doeven MK, Poolman B. ABC transporter architecture and regulatory roles of accessory domains. FEBS Lett. 2006;580(4):1023-1035.
Sikkema HR, van den Noort M, Rheinberger J, et al. Gating by ionic strength and safety check by cyclic-di-AMP in the ABC transporter OpuA. Sci Adv. 2020;6(47):eabd7697.
Hwang TC, Braakman I, van der Sluijs P, Callebaut I. Structure basis of CFTR folding, function and pharmacology. J Cyst Fibros. 2023;22(suppl 1):S5-S11.
Coleman JA, Quazi F, Molday RS. Mammalian P4-ATPases and ABC transporters and their role in phospholipid transport. Biochim Biophys Acta. 2013;1831(3):555-574.
Lyons JA, Timcenko M, Dieudonné T, Lenoir G, Nissen P. P4-ATPases: how an old dog learnt new tricks-structure and mechanism of lipid flippases. Curr Opin Struct Biol. 2020;63:65-73.
Wong LH, Gatta AT, Levine TP. Lipid transfer proteins: the lipid commute via shuttles, bridges and tubes. Nat Rev Mol Cell Biol. 2019;20(2):85-101.
Wong LH, Levine TP. Tubular lipid binding proteins (TULIPs) growing everywhere. Biochim Biophys Acta Mol Cell Res. 2017;1864(9):1439-1449.
Corbalan-Garcia S, Gómez-Fernández JC. Signaling through C2 domains: more than one lipid target. Biochim Biophys Acta. 2014;1838(6):1536-1547.
Lemmon MA. Membrane recognition by phospholipid-binding domains. Nat Rev Mol Cell Biol. 2008;9(2):99-111.
Malcova I, Bumba L, Uljanic F, Kuzmenko D, Nedomova J, Kamanova J. Lipid binding by the N-terminal motif mediates plasma membrane localization of Bordetella effector protein BteA. J Biol Chem. 2021;296:100607.
Varela-Chavez C, Blondel A, Popoff MR. Bacterial intracellularly active toxins: membrane localisation of the active domain. Cell Microbiol. 2020;22(7):e13213.
López-Lara IM, Geiger O. Bacterial lipid diversity. Biochim Biophys Acta Mol Cell Biol Lipids. 2017;1862(11):1287-1299.
Petroutsos D, Amiar S, Abida H, et al. Evolution of galactoglycerolipid biosynthetic pathways-from cyanobacteria to primary plastids and from primary to secondary plastids. Prog Lipid Res. 2014;54:68-85.
Wada H, Murata N. Membrane lipids in cyanobacteria. In: Siegenthaler P-A, Murata N, eds. Lipids in Photosynthesis. Kluwer Academic Publishers; 1998:65-81.
Boudière L, Michaud M, Petroutsos D, et al. Glycerolipids in photosynthesis: composition, synthesis and trafficking. Biochim Biophys Acta. 2014;1837(4):470-480.
Wada H, Murata N. The essential role of phosphatidylglycerol in photosynthesis. Photosynth Res. 2007;92(2):205-215.
Kóbori TO, Uzumaki T, Kis M, et al. Phosphatidylglycerol is implicated in divisome formation and metabolic processes of cyanobacteria. J Plant Physiol. 2018;223:96-104.
Terrapon N, Weiner J, Grath S, Moore AD, Bornberg-Bauer E. Rapid similarity search of proteins using alignments of domain arrangements. Bioinformatics. 2014;30(2):274-281.
Buchan DWA, Jones DT. Learning a functional grammar of protein domains using natural language word embedding techniques. Proteins. 2020;88(4):616-624.