Annexins are Ca2+-binding, membrane-interacting proteins, widespread among eukaryotes, consisting usually of four structurally similar repeated domains. It is accepted that vertebrate annexins derive from a double genome duplication event. It has been postulated that a single domain annexin, if found, might represent a molecule related to the hypothetical ancestral annexin. The recent discovery of a single-domain annexin in a bacterium, Cytophaga hutchinsonii, apparently confirmed this hypothesis. Here, we present a more complex picture. Using remote sequence similarity detection tools, a survey of bacterial genomes was performed in search of annexin-like proteins. In total, we identified about thirty annexin homologues, including single-domain and multi-domain annexins, in seventeen bacterial species. The thorough search yielded, besides the known annexin homologue from C. hutchinsonii, homologues from the Bacteroidetes/Chlorobi phylum, from Gemmatimonadetes, from beta- and delta-Proteobacteria, and from Actinobacteria. The sequences of bacterial annexins exhibited remote but statistically significant similarity to sequence profiles built of the eukaryotic ones. Some bacterial annexins are equipped with additional, different domains, for example those characteristic for toxins. The variation in bacterial annexin sequences, much wider than that observed in eukaryotes, and different domain architectures suggest that annexins found in bacteria may actually descend from an ancestral bacterial annexin, from which eukaryotic annexins also originate. The hypothesis of an ancient origin of bacterial annexins has to be reconciled with the fact that remarkably few bacterial strains possess annexin genes compared to the thousands of known bacterial genomes and with the patchy, anomalous phylogenetic distribution of bacterial annexins. Thus, a massive annexin gene loss in several bacterial lineages or very divergent evolution would appear a likely explanation. Alternative evolutionary scenarios, involving horizontal gene transfer between bacteria and protozoan eukaryotes, in either direction, appear much less likely. Altogether, current evidence does not allow unequivocal judgement as to the origin of bacterial annexins.
References
[1]
Gerke V, Moss SE (2002) Annexins: from structure to function. Physiol Rev 82(2): 331–371.
[2]
Barton GJ, Newman RH, Freemont PS, Crumpton MJ (1991) Amino acid sequence analysis of the annexin super-gene family of proteins. Eur J Biochem 198(3): 749–760.
[3]
Clark GB, Roux SJ (1995) Annexins of plant cells. Plant Physiol 109(4): 1133–1139.
[4]
Morgan RO, Fernandez MP (1995) Molecular phylogeny of annexins and identification of a primitive homologue in Giardia lamblia. Mol Biol Evol 12(6): 967–979.
[5]
Swairjo MA, Seaton BA (1994) Annexin structure and membrane interactions: a molecular perspective. Annu Rev Biophys Biomol Struct 23: 193–213.
Rescher U, Gerke V (2004) Annexins–unique membrane binding proteins with diverse functions. J Cell Sci 117(Pt 13): 2631–2639.
[8]
Talukdar T, Gorecka KM, de Carvalho-Niebel F, Downie JA, Cullimore J, et al. (2009) Annexins - calcium- and membrane-binding proteins in the plant kingdom: potential role in nodulation and mycorrhization in Medicago truncatula. Acta Biochim Pol 56(2): 199–210.
[9]
Laohavisit A, Davies JM (2011) Annexins. New Phytol 189(1): 40–53.
[10]
Clark GB, Morgan RO, Fernandez MP, Roux SJ (2012) Evolutionary adaptation of plant annexins has diversified their molecular structures, interactions and functional roles. New Phytol 196: 695–712.
[11]
Smith PD, Moss SE (1994) Structural evolution of the annexin supergene family. Trends Genet 10(7): 241–246.
[12]
Moss SE, Morgan RO (2004) The annexins. Genome Biol 5(4): 219.
[13]
Morgan RO, Pilar Fernandez M (1997) Distinct annexin subfamilies in plants and protists diverged prior to animal annexins and from a common ancestor. J Mol Evol 44(2): 178–188.
[14]
Morgan RO, Martin-Almedina S, Garcia M, Jhoncon-Kooyip J, Fernandez MP (2006) Deciphering function and mechanism of calcium-binding proteins from their evolutionary imprints. Biochim Biophys Acta 1763(11): 1238–1249.
[15]
Cantacessi C, Seddon JM, Miller TL, Leow CY, Thomas L, et al. (2013) A genome-wide analysis of annexins from parasitic organisms and their vectors. Sci Rep 3: 2893.
[16]
Soding J, Biegert A, Lupas AN (2005) The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res 33(Web Server issue): W244–248.
[17]
Jaroszewski L, Li Z, Cai XH, Weber C, Godzik A (2011) FFAS server: novel features and applications. Nucleic Acids Res 39 Suppl 2W38–44.
[18]
Finn RD, Clements J, Eddy SR (2011) HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 39(Web Server issue): W29–37.
[19]
Pruitt KD, Tatusova T, Brown GR, Maglott DR (2012) NCBI Reference Sequences (RefSeq): current status, new features and genome annotation policy. Nucleic Acids Res 40(Database issue): D130–135.
[20]
Marcotte EM, Pellegrini M, Thompson MJ, Yeates TO, Eisenberg D (1999) A combined algorithm for genome-wide prediction of protein function. Nature 402(6757): 83–86.
[21]
Ferrer L, Dale JM, Karp PD (2010) A systematic study of genome context methods: calibration, normalization and combination. BMC Bioinformatics 11: 493.
[22]
Huber R, Romisch J, Paques EP (1990) The crystal and molecular structure of human annexin V, an anticoagulant protein that binds to calcium and membranes. Embo J 9(12): 3867–3874.
Hofmann A, Raguenes-Nicol C, Favier-Perron B, Mesonero J, Huber R, et al. (2000) The annexin A3-membrane interaction is modulated by an N-terminal tryptophan. Biochemistry 39(26): 7712–7721.
[25]
McDaniel LD, Young EC, Ritchie KB, Paul JH (2012) Environmental factors influencing gene transfer agent (GTA) mediated transduction in the subtropical ocean. PLoS One 7(8): e43506.
[26]
Frickey T, Lupas A (2004) CLANS: a Java application for visualizing protein families based on pairwise similarity. Bioinformatics 20(18): 3702–3704.
[27]
Paul C, Pohnert G (2012) Interactions of the algicidal bacterium Kordia algicida with diatoms: regulated protease excretion for specific algal lysis. PLoS One 6(6): e21032.
[28]
Nakayama H, Fukuda S, Inoue H, Nishida-Fukuda H, Shirakata Y, et al. (2012) Cell surface annexins regulate ADAM-mediated ectodomain shedding of proamphiregulin. Mol Biol Cell 23(10): 1964–1975.
[29]
Hansen SK, Rainey PB, Haagensen JA, Molin S (2007) Evolution of species interactions in a biofilm community. Nature 445(7127): 533–536.
[30]
Huang R, Li M, Gregory RL (2011) Bacterial interactions in dental biofilm. Virulence 2(5): 435–444.
[31]
Teles FR, Teles RP, Uzel NG, Song XQ, Torresyap G, et al. (2012) Early microbial succession in redeveloping dental biofilms in periodontal health and disease. J Periodontal Res 47(1): 95–104.
[32]
Lang E, Stackebrandt E (2009) Emended descriptions of the genera Myxococcus and Corallococcus, typification of the species Myxococcus stipitatus and Myxococcus macrosporus and a proposal that they be represented by neotype strains. Request for an Opinion. Int J Syst Evol Microbiol 59(Pt 8): 2122–2128.
[33]
Yajima S, Nakanishi K, Takahashi K, Ogawa T, Hidaka M, et al. (2004) Relation between tRNase activity and the structure of colicin D according to X-ray crystallography. Biochem Biophys Res Commun 322(3): 966–973.
[34]
Soelaiman S, Jakes K, Wu N, Li C, Shoham M (2001) Crystal structure of colicin E3: implications for cell entry and ribosome inactivation. Mol Cell 8(5): 1053–1062.
[35]
Bandorowicz-Pikula J, Wos M, Pikula S (2012) Do annexins participate in lipid messenger mediated intracellular signaling? A question revisited. Mol Membr Biol 29: 229–242.
[36]
Zhang D, de Souza RF, Anantharaman V, Iyer LM, Aravind L (2012) Polymorphic toxin systems: Comprehensive characterization of trafficking modes, processing, mechanisms of action, immunity and ecology using comparative genomics. Biol Direct 7: 18.
[37]
Hayes MJ, Rescher U, Gerke V, Moss SE (2004) Annexin-actin interactions. Traffic 5(8): 571–576.
[38]
Grieve AG, Moss SE, Hayes MJ (2012) Annexin A2 at the interface of actin and membrane dynamics: a focus on its roles in endocytosis and cell polarization. Int J Cell Biol 2012: 852430.
[39]
Ivanova N, Daum C, Lang E, Abt B, Kopitz M, et al. (2010) Complete genome sequence of Haliangium ochraceum type strain (SMP-2). Stand Genomic Sci 2(1): 96–106.
[40]
Kondo N, Nikoh N, Ijichi N, Shimada M, Fukatsu T (2002) Genome fragment of Wolbachia endosymbiont transferred to X chromosome of host insect. Proc Natl Acad Sci U S A 99(22): 14280–14285.
[41]
Dunning Hotopp JC, Clark ME, Oliveira DC, Foster JM, Fischer P, et al. (2007) Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes. Science 317(5845): 1753–1756.
[42]
Nikoh N, Tanaka K, Shibata F, Kondo N, Hizume M, et al. (2008) Wolbachia genome integrated in an insect chromosome: evolution and fate of laterally transferred endosymbiont genes. Genome Res 18(2): 272–280.
[43]
Dunning Hotopp JC (2011) Horizontal gene transfer between bacteria and animals. Trends Genet 27(4): 157–163.
[44]
Liu H, Fu Y, Li B, Yu X, Xie J, et al. (2011) Widespread Horizontal Gene Transfer from Circular Single-stranded DNA Viruses to Eukaryotic Genomes. BMC Evol Biol 11(1): 276.
[45]
Pawlowski K, Muszewska A, Lenart A, Szczepinska T, Godzik A, et al. (2010) A widespread peroxiredoxin-like domain present in tumor suppression- and progression-implicated proteins. BMC Genomics 11: 590.
[46]
Lenart A, Dudkiewicz M, Grynberg M, Pawlowski K (2013) CLCAs - a family of metalloproteases of intriguing phylogenetic distribution and with recurring inactive active sites. PLoS One 8: e62272.
[47]
Cerda-Costa N, Guevara T, Karim AY, Ksiazek M, Nguyen KA, et al. (2011) The structure of the catalytic domain of Tannerella forsythia karilysin reveals it is a bacterial xenologue of animal matrix metalloproteinases. Mol Microbiol 79(1): 119–132.
[48]
Goulas T, Arolas JL, Gomis-Ruth FX (2011) Structure, function and latency regulation of a bacterial enterotoxin potentially derived from a mammalian adamalysin/ADAM xenolog. Proc Natl Acad Sci U S A 108(5): 1856–1861.
[49]
Dana CE, Glauber KM, Chan TA, Bridge DM, Steele RE (2012) Incorporation of a horizontally transferred gene into an operon during cnidarian evolution. PLoS One 7(2): e31643.
[50]
Steczkiewicz K, Muszewska A, Knizewski L, Rychlewski L, Ginalski K (2012) Sequence, structure and functional diversity of PD-(D/E)XK phosphodiesterase superfamily. Nucleic Acids Res 40(15): 7016–7045.
[51]
Schoenfeld TW, Murugapiran SK, Dodsworth JA, Floyd S, Lodes M, et al. (2013) Lateral Gene Transfer of Family A DNA Polymerases between Thermophilic Viruses, Aquificae, and Apicomplexa. Mol Biol Evol 30(7): 1653–1664.
[52]
Podell S, Gaasterland T, Allen EE (2008) A database of phylogenetically atypical genes in archaeal and bacterial genomes, identified using the DarkHorse algorithm. BMC Bioinformatics 9: 419.
[53]
Johnson LS, Eddy SR, Portugaly E (2010) Hidden Markov model speed heuristic and iterative HMM search procedure. BMC Bioinformatics 11: 431.
[54]
Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, et al.. (2012) The Pfam protein families database. Nucleic Acids Res 40(Database issue): D290–301.
[55]
Rychlewski L, Jaroszewski L, Li W, Godzik A (2000) Comparison of sequence profiles. Strategies for structural predictions using sequence information. Protein Sci 9(2): 232–241.
[56]
Soding J (2005) Protein homology detection by HMM-HMM comparison. Bioinformatics 21(7): 951–960.
[57]
Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25(17): 3389–3402.
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32(5): 1792–1797.
[60]
Pei J, Kim BH, Grishin NV (2008) PROMALS3D: a tool for multiple protein sequence and structure alignments. Nucleic Acids Res 36(7): 2295–2300.
[61]
McGuffin LJ, Bryson K, Jones DT (2000) The PSIPRED protein structure prediction server. Bioinformatics 16(4): 404–405.
[62]
Cole C, Barber JD, Barton GJ (2008) The Jpred 3 secondary structure prediction server. Nucleic Acids Res 36(Web Server issue): W197–201.
[63]
Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, et al.. (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 36(Web Server issue): W465–469.
[64]
Crooks GE, Hon G, Chandonia JM, Brenner SE (2004) WebLogo: a sequence logo generator. Genome Res 14(6): 1188–1190.
[65]
Waterhouse AM, Procter JB, Martin DM, Clamp M, Barton GJ (2009) Jalview Version 2–a multiple sequence alignment editor and analysis workbench. Bioinformatics 25(9): 1189–1191.
[66]
Hall T (2012) BioEdit. Available: http://www.mbio.ncsu.edu/BioEdit/bioedit？.html. Accessed 2012.
[67]
Sonnhammer EL, von Heijne G, Krogh A (1998) A hidden Markov model for predicting transmembrane helices in protein sequences. Proc Int Conf Intell Syst Mol Biol 6: 175–182.
[68]
Kall L, Krogh A, Sonnhammer EL (2007) Advantages of combined transmembrane topology and signal peptide prediction–the Phobius web server. Nucleic Acids Res 35(Web Server issue): W429–432.
[69]
Li W, Godzik A (2006) Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22(13): 1658–1659.
[70]
Katoh K, Misawa K, Kuma K, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30(14): 3059–3066.
[71]
Capella-Gutierrez S, Silla-Martinez JM, Gabaldon T (2009) trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25(15): 1972–1973.
[72]
Benson DA, Cavanaugh M, Clark K, Karsch-Mizrachi I, Lipman DJ, et al. (2013) GenBank. Nucleic Acids Res 41(D1): D36–42.
[73]
Pagani I, Liolios K, Jansson J, Chen IM, Smirnova T, et al.. (2012) The Genomes OnLine Database (GOLD) v.4: status of genomic and metagenomic projects and their associated metadata. Nucleic Acids Res 40(Database issue): D571–579.
[74]
Dehal PS, Joachimiak MP, Price MN, Bates JT, Baumohl JK, et al.. (2010) MicrobesOnline: an integrated portal for comparative and functional genomics. Nucleic Acids Res 38(Database issue): D396–400.
[75]
Lin B, Lu G, Zheng Y, Xie W, Li S, et al. (2012) Aquimarina agarilytica sp. nov., an agarolytic species isolated from a red alga. Int J Syst Evol Microbiol 62(Pt 4): 869–873.
[76]
Smith J, Lewis GD (2007) Bacterially mediated manganese deposition in novel ‘anelli’within the biofilms of an impacted urban stream.
[77]
Leadbetter ER, Holt SC, Socransky SS (1979) Capnocytophaga: new genus of gram-negative gliding bacteria. I. General characteristics, taxonomic considerations and significance. Arch Microbiol 122(1): 9–16.
[78]
Huntley S, Zhang Y, Treuner-Lange A, Kneip S, Sensen CW, et al. (2012) Complete genome sequence of the fruiting myxobacterium Corallococcus coralloides DSM 2259. J Bacteriol 194(11): 3012–3013.
[79]
Xie G, Bruce DC, Challacombe JF, Chertkov O, Detter JC, et al. (2007) Genome sequence of the cellulolytic gliding bacterium Cytophaga hutchinsonii. Appl Environ Microbiol 73(11): 3536–3546.
[80]
Filippini M, Qi W, Jaenicke S, Goesmann A, Smits TH, et al. (2012) Genome sequence of the filamentous bacterium Fibrisoma limi BUZ 3T. J Bacteriol 194(16): 4445.
[81]
Du Z, Zhang Z, Miao T, Wu J, Lu G, et al. (2011) Draft genome sequence of the novel agar-digesting marine bacterium HQM9. J Bacteriol 193(17): 4557–4558.
[82]
Nupur, Sharma S, Kumar Singh P, Suresh K, Anil Kumar P (2012) Fulvivirga imtechensis sp. nov., a member of the phylum Bacteroidetes. Int J Syst Evol Microbiol 62(Pt 9): 2213–2217.
[83]
Zhang H, Sekiguchi Y, Hanada S, Hugenholtz P, Kim H, et al. (2003) Gemmatimonas aurantiaca gen. nov., sp. nov., a gram-negative, aerobic, polyphosphate-accumulating micro-organism, the first cultured representative of the new bacterial phylum Gemmatimonadetes phyl. nov. Int J Syst Evol Microbiol 53(Pt 4): 1155–1163.
[84]
Lee HS, Kang SG, Kwon KK, Lee JH, Kim SJ (2011) Genome sequence of the algicidal bacterium Kordia algicida OT-1. J Bacteriol 193(15): 4031–4032.
[85]
Kumar S, Subramanian S, Raghava GP, Pinnaka AK (2012) Genome sequence of the marine bacterium Marinilabilia salmonicolor JCM 21150T. J Bacteriol 194(14): 3746.
[86]
Nakagawa Y, Sakane T, Suzuki M, Hatano K (2002) Phylogenetic structure of the genera Flexibacter, Flexithrix, and Microscilla deduced from 16S rRNA sequence analysis. J Gen Appl Microbiol 48(3): 155–165.
[87]
Tice H, Mayilraj S, Sims D, Lapidus A, Nolan M, et al. (2010) Complete genome sequence of Nakamurella multipartita type strain (Y-104). Stand Genomic Sci 2(2): 168–175.
[88]
Vikram S, Kumar S, Subramanian S, Raghava GP (2012) Draft genome sequence of the nitrophenol-degrading actinomycete Rhodococcus imtechensis RKJ300. J Bacteriol 194(13): 3543.
[89]
Lail K, Sikorski J, Saunders E, Lapidus A, Glavina Del Rio T, et al. (2010) Complete genome sequence of Spirosoma linguale type strain (1). Stand Genomic Sci 2(2): 176–185.
