Mapping glycoprotein structure reveals Flaviviridae evolutionary history.
Journal
Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462
Informations de publication
Date de publication:
04 Sep 2024
04 Sep 2024
Historique:
received:
10
02
2024
accepted:
01
08
2024
medline:
5
9
2024
pubmed:
5
9
2024
entrez:
4
9
2024
Statut:
aheadofprint
Résumé
Viral glycoproteins drive membrane fusion in enveloped viruses and determine host range, tissue tropism and pathogenesis
Identifiants
pubmed: 39232167
doi: 10.1038/s41586-024-07899-8
pii: 10.1038/s41586-024-07899-8
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2024. The Author(s).
Références
Grove, J. & Marsh, M. The cell biology of receptor-mediated virus entry. J. Cell Biol. 195, 1071–1082 (2011).
pubmed: 22123832
pmcid: 3246895
doi: 10.1083/jcb.201108131
Simmonds, P. et al. ICTV virus taxonomy profile: Flaviviridae. J. Gen. Virol. 98, 2–3 (2017).
pubmed: 28218572
pmcid: 5370391
doi: 10.1099/jgv.0.000672
Rey, F. A. & Lok, S.-M. Common features of enveloped viruses and implications for immunogen design for next-generation vaccines. Cell 172, 1319–1334 (2018).
pubmed: 29522750
pmcid: 7112304
doi: 10.1016/j.cell.2018.02.054
Hubálek, Z. & Halouzka, J. West Nile fever—a reemerging mosquito-borne viral disease in Europe. Emerg. Infect. Dis. 5, 643–650 (1999).
pubmed: 10511520
pmcid: 2627720
doi: 10.3201/eid0505.990505
Wang, Z.-D. et al. A new segmented virus associated with human febrile illness in China. N. Engl. J. Med. 380, 2116–2125 (2019).
pubmed: 31141633
doi: 10.1056/NEJMoa1805068
Kartashov, M. Y. et al. Novel Flavi-like virus in ixodid ticks and patients in Russia. Ticks Tick Borne Dis. 14, 102101 (2023).
pubmed: 36529011
doi: 10.1016/j.ttbdis.2022.102101
Postler, T. S. et al. Renaming of the genus Flavivirus to Orthoflavivirus and extension of binomial species names within the family Flaviviridae. Arch. Virol 168, 224 (2023).
pubmed: 37561168
doi: 10.1007/s00705-023-05835-1
Qin, X.-C. et al. A tick-borne segmented RNA virus contains genome segments derived from unsegmented viral ancestors. Proc. Natl Acad. Sci. USA 111, 6744–6749 (2014).
pubmed: 24753611
pmcid: 4020047
doi: 10.1073/pnas.1324194111
Ladner, J. T. et al. A multicomponent animal virus isolated from mosquitoes. Cell Host Microbe 20, 357–367 (2016).
pubmed: 27569558
pmcid: 5025392
doi: 10.1016/j.chom.2016.07.011
Paraskevopoulou, S. et al. Viromics of extant insect orders unveil the evolution of the flavi-like superfamily. Virus Evol. 7, veab030 (2021).
pubmed: 34026271
pmcid: 8129625
doi: 10.1093/ve/veab030
Kobayashi, K. et al. Gentian Kobu-sho-associated virus: a tentative, novel double-stranded RNA virus that is relevant to gentian Kobu-sho syndrome. J. Gen. Plant Pathol. 79, 56–63 (2013).
doi: 10.1007/s10327-012-0423-5
Debat, H. & Bejerman, N. Two novel flavi-like viruses shed light on the plant-infecting koshoviruses. Arch. Virol 168, 184 (2023).
pubmed: 37338667
doi: 10.1007/s00705-023-05813-7
Petrone, M. E. et al. A ~40-kb flavi-like virus does not encode a known error-correcting mechanism. Proc. Natl Acad. Sci. USA 121, e2403805121 (2024).
Ferron, F., Sama, B., Decroly, E. & Canard, B. The enzymes for genome size increase and maintenance of large (+)RNA viruses. Trends Biochem. Sci 46, 866–877 (2021).
pubmed: 34172362
doi: 10.1016/j.tibs.2021.05.006
Shi, M. et al. Divergent viruses discovered in arthropods and vertebrates revise the evolutionary history of the Flaviviridae and related viruses. J. Virol. 90, 659–669 (2016).
pubmed: 26491167
doi: 10.1128/JVI.02036-15
Garry, C. E. & Garry, R. F. Proteomics computational analyses suggest that the envelope glycoproteins of segmented Jingmen Flavi-like viruses are class II viral fusion proteins (b-penetrenes) with mucin-like domains. Viruses 12, 260 (2020).
pubmed: 32120884
pmcid: 7150890
doi: 10.3390/v12030260
Jumper, J. et al. Highly accurate protein structure prediction with AlphaFold. Nature 596, 583–589 (2021).
pubmed: 34265844
pmcid: 8371605
doi: 10.1038/s41586-021-03819-2
Lin, Z. et al. Evolutionary-scale prediction of atomic-level protein structure with a language model. Science 379, 1123–1130 (2023).
pubmed: 36927031
doi: 10.1126/science.ade2574
Mirdita, M. et al. ColabFold: making protein folding accessible to all. Nat. Methods 19, 679–682 (2022).
pubmed: 35637307
pmcid: 9184281
doi: 10.1038/s41592-022-01488-1
Lee, S. et al. Petascale Homology Search for Structure Prediction. Preprint at bioRxiv https://doi.org/10.1101/2023.07.10.548308 (2023).
Blitvich, B. J. & Firth, A. E. A review of Flaviviruses that have no known arthropod vector. Viruses 9, 154 (2017).
pubmed: 28635667
pmcid: 5490829
doi: 10.3390/v9060154
Kielian, M. & Rey, F. A. Virus membrane-fusion proteins: more than one way to make a hairpin. Nat. Rev. Microbiol. 4, 67–76 (2006).
pubmed: 16357862
pmcid: 7097298
doi: 10.1038/nrmicro1326
Rey, F. A., Heinz, F. X., Mandl, C., Kunz, C. & Harrison, S. C. The envelope glycoprotein from tick-borne encephalitis virus at 2 Å resolution. Nature 375, 291–298 (1995).
pubmed: 7753193
doi: 10.1038/375291a0
Dessau, M. & Modis, Y. Crystal structure of glycoprotein C from Rift Valley fever virus. Proc. Natl Acad. Sci. USA 110, 1696–1701 (2013).
pubmed: 23319635
pmcid: 3562824
doi: 10.1073/pnas.1217780110
Fédry, J. et al. The ancient gamete fusogen HAP2 is a eukaryotic class II fusion protein. Cell 168, 904–915.e10 (2017).
pubmed: 28235200
pmcid: 5332557
doi: 10.1016/j.cell.2017.01.024
Guardado-Calvo, P. & Rey, F. A. The viral class II membrane fusion machinery: divergent evolution from an ancestral heterodimer. Viruses 13, 2368 (2021).
pubmed: 34960636
pmcid: 8706100
doi: 10.3390/v13122368
Li, L. et al. The flavivirus precursor membrane-envelope protein complex: structure and maturation. Science 319, 1830–1834 (2008).
pubmed: 18369147
doi: 10.1126/science.1153263
El Omari, K., Iourin, O., Harlos, K., Grimes, J. M. & Stuart, D. I. Structure of a Pestivirus envelope glycoprotein E2 clarifies its role in cell entry. Cell Rep. 3, 30–35 (2013).
pubmed: 23273918
pmcid: 3607223
doi: 10.1016/j.celrep.2012.12.001
Li, Y., Wang, J., Kanai, R. & Modis, Y. Crystal structure of glycoprotein E2 from bovine viral diarrhea virus. Proc. Natl Acad. Sci. USA 110, 6805–6810 (2013).
pubmed: 23569276
pmcid: 3637714
doi: 10.1073/pnas.1300524110
Kong, L. et al. Hepatitis C virus E2 envelope glycoprotein core structure. Science 342, 1090–1094 (2013).
pubmed: 24288331
pmcid: 3954638
doi: 10.1126/science.1243876
Khan, A. G. et al. Structure of the core ectodomain of the hepatitis C virus envelope glycoprotein 2. Nature 509, 381–384 (2014).
pubmed: 24553139
pmcid: 4126800
doi: 10.1038/nature13117
Aitkenhead, H. et al. Structural comparison of typical and atypical E2 Pestivirus glycoproteins. Structure 32, 273–281 (2024).
pubmed: 38176409
doi: 10.1016/j.str.2023.12.003
Torrents de la Peña, A. et al. Structure of the hepatitis C virus E1E2 glycoprotein complex. Science 378, 263–269 (2022).
pubmed: 36264808
doi: 10.1126/science.abn9884
Metcalf, M. C. et al. Structure of engineered hepatitis C virus E1E2 ectodomain in complex with neutralizing antibodies. Nat. Commun. 14, 3980 (2023).
pubmed: 37407593
pmcid: 10322937
doi: 10.1038/s41467-023-39659-z
van Kempen, M. et al. Fast and accurate protein structure search with Foldseek. Nat. Biotechnol. 42, 243–246 (2024).
pubmed: 37156916
doi: 10.1038/s41587-023-01773-0
Oliver, M. R. et al. Structures of the hepaci-, pegi-, and pestiviruses envelope proteins suggest a novel membrane fusion mechanism. PLoS Biol. 21, e3002174 (2023).
pubmed: 37432947
pmcid: 10335668
doi: 10.1371/journal.pbio.3002174
Buchfink, B., Reuter, K. & Drost, H.-G. Sensitive protein alignments at tree-of-life scale using DIAMOND. Nat. Methods 18, 366–368 (2021).
pubmed: 33828273
pmcid: 8026399
doi: 10.1038/s41592-021-01101-x
Jones, P. et al. InterProScan 5: genome-scale protein function classification. Bioinformatics 30, 1236–1240 (2014).
pubmed: 24451626
pmcid: 3998142
doi: 10.1093/bioinformatics/btu031
Urayama, S.-I., Takaki, Y. & Nunoura, T. FLDS: a comprehensive dsRNA sequencing method for intracellular RNA virus surveillance. Microbes Environ. 31, 33–40 (2016).
pubmed: 26877136
pmcid: 4791113
doi: 10.1264/jsme2.ME15171
Hou, X. et al. Artificial intelligence redefines RNA virus discovery. Preprint at bioRxiv https://doi.org/10.1101/2023.04.18.537342 (2023).
Chen, Y.-M. et al. RNA viromes from terrestrial sites across China expand environmental viral diversity. Nat. Microbiol. 7, 1312–1323 (2022).
pubmed: 35902778
doi: 10.1038/s41564-022-01180-2
Arhab, Y., Bulakhov, A. G., Pestova, T. V. & Hellen, C. U. T. Dissemination of internal ribosomal entry sites (IRES) between viruses by horizontal gene transfer. Viruses 12, 612 (2020).
pubmed: 32512856
pmcid: 7354566
doi: 10.3390/v12060612
Modis, Y., Ogata, S., Clements, D. & Harrison, S. C. Structure of the dengue virus envelope protein after membrane fusion. Nature 427, 313–319 (2004).
pubmed: 14737159
doi: 10.1038/nature02165
MacIntosh, G. C. in Ribonucleases (ed. Nicholson, A. W.) 89–114 (Springer, 2011).
Puente-Lelievre, C. et al. Tertiary-interaction characters enable fast, model-based structural phylogenetics beyond the twilight zone. Preprint at bioRxiv https://doi.org/10.1101/2023.12.12.571181 (2024).
Vaney, M.-C. et al. Evolution and activation mechanism of the flavivirus class II membrane-fusion machinery. Nat. Commun. 13, 3718 (2022).
pubmed: 35764616
pmcid: 9239988
doi: 10.1038/s41467-022-31111-y
Bamford, C. G. G., de Souza, W. M., Parry, R. & Gifford, R. J. Comparative analysis of genome-encoded viral sequences reveals the evolutionary history of flavivirids (family Flaviviridae). Virus Evol. 8, veac085 (2022).
pubmed: 36533146
pmcid: 9752770
doi: 10.1093/ve/veac085
Mushegian, A. Methyltransferases of Riboviria. Biomolecules 12, 1247 (2022).
pubmed: 36139088
pmcid: 9496149
doi: 10.3390/biom12091247
Li, Z., Jaroszewski, L., Iyer, M., Sedova, M. & Godzik, A. FATCAT 2.0: towards a better understanding of the structural diversity of proteins. Nucleic Acids Res. 48, 60–64 (2020).
doi: 10.1093/nar/gkaa443
Mifsud, J. C. O. et al. Transcriptome mining extends the host range of the Flaviviridae to non-bilaterians. Virus Evol. 9, veac124 (2022).
pubmed: 36694816
pmcid: 9854234
doi: 10.1093/ve/veac124
Kong, Y. et al. Metatranscriptomics reveals the diversity of the tick virome in northwest China. Microbiol. Spectr. 10, e0111522 (2022).
pubmed: 36214702
doi: 10.1128/spectrum.01115-22
Costa, V. A. et al. Limited cross-species virus transmission in a spatially restricted coral reef fish community. Virus Evol. 9, vead011 (2023).
pubmed: 36910859
pmcid: 9994595
doi: 10.1093/ve/vead011
Perveen, N. et al. Virome diversity of Hyalomma dromedarii ticks collected from camels in the United Arab Emirates. Vet World 16, 439–448 (2023).
pubmed: 37041826
pmcid: 10082741
doi: 10.14202/vetworld.2023.439-448
Guo, G. et al. Virome analysis provides an insight into the viral community of Chinese mitten crab Eriocheir sinensis. Microbiol. Spectr. 11, e0143923 (2023).
pubmed: 37358426
doi: 10.1128/spectrum.01439-23
Dunay, E. et al. Viruses in sanctuary chimpanzees across Africa. Am. J. Primatol. 85, e23452 (2023).
pubmed: 36329642
doi: 10.1002/ajp.23452
Elbadry, M. A. et al. Diversity and genetic reassortment of keystone virus in mosquito populations in Florida. Am. J. Trop. Med. Hyg. 108, 1256–1263 (2023).
pubmed: 37127267
pmcid: 10540117
doi: 10.4269/ajtmh.22-0594
Fu, L., Niu, B., Zhu, Z., Wu, S. & Li, W. CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics 28, 3150–3152 (2012).
pubmed: 23060610
pmcid: 3516142
doi: 10.1093/bioinformatics/bts565
Kearse, M. et al. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647–1649 (2012).
pubmed: 22543367
pmcid: 3371832
doi: 10.1093/bioinformatics/bts199
Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772–780 (2013).
pubmed: 23329690
pmcid: 3603318
doi: 10.1093/molbev/mst010
Edgar, R. C. et al. Petabase-scale sequence alignment catalyses viral discovery. Nature 602, 142–147 (2022).
pubmed: 35082445
doi: 10.1038/s41586-021-04332-2
Mifsud, J. C. O. BatchArtemisSRAMiner: v1.0.0. Zenodo https://doi.org/10.5281/zenodo.8417951 (2023).
Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014).
pubmed: 24695404
pmcid: 4103590
doi: 10.1093/bioinformatics/btu170
Li, D., Liu, C.-M., Luo, R., Sadakane, K. & Lam, T.-W. MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph. Bioinformatics 31, 1674–1676 (2015).
pubmed: 25609793
doi: 10.1093/bioinformatics/btv033
Teufel, F. et al. SignalP 6.0 predicts all five types of signal peptides using protein language models. Nat. Biotechnol. 40, 1023–1025 (2022).
pubmed: 34980915
pmcid: 9287161
doi: 10.1038/s41587-021-01156-3
Edgar, R. C. Muscle5: high-accuracy alignment ensembles enable unbiased assessments of sequence homology and phylogeny. Nat. Commun. 13, 6968 (2022).
pubmed: 36379955
pmcid: 9664440
doi: 10.1038/s41467-022-34630-w
Mifsud, J. C. O. et al. Underlying data for “Mapping glycoprotein structure reveals Flaviviridae evolutionary history”. Zenodo https://doi.org/10.5281/zenodo.11092288 (2024).
Meng, E. C. et al. UCSF ChimeraX: tools for structure building and analysis. Protein Sci. 32, e4792 (2023).
pubmed: 37774136
pmcid: 10588335
doi: 10.1002/pro.4792
Letunic, I. & Bork, P. Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res. 49, 293–296 (2021).
doi: 10.1093/nar/gkab301
Renner, M. et al. Flavivirus maturation leads to the formation of an occupied lipid pocket in the surface glycoproteins. Nat. Commun. 12, 1238 (2021).
pubmed: 33623019
pmcid: 7902656
doi: 10.1038/s41467-021-21505-9
Egloff, M.-P., Benarroch, D., Selisko, B., Romette, J.-L., & Canard, B. An RNA cap (nucleoside-2′-O-)-methyltransferase in the flavivirus RNA polymerase NS5: crystal structure and functional characterization. EMBO J. 21, 2757–2768 (2002).
pubmed: 12032088
pmcid: 125380
doi: 10.1093/emboj/21.11.2757
Noble, C. G. et al. A conserved pocket in the dengue virus polymerase identified through fragment-based screening. J. Biol. Chem. 291, 8541–8548 (2016).
pubmed: 26872970
pmcid: 4861426
doi: 10.1074/jbc.M115.710731
Jia, H., Zhong, Y., Peng, C. & Gong, P. Crystal structures of flavivirus NS5 guanylyltransferase reveal a GMP-arginine adduct. J. Virol. 96, e0041822 (2022).
pubmed: 35758665
doi: 10.1128/jvi.00418-22
Walls, A. C. et al. Structure, function, and antigenicity of the SARS-CoV-2 spike glycoprotein. Cell 181, 281–292 (2020).
pubmed: 32155444
pmcid: 7102599
doi: 10.1016/j.cell.2020.02.058
Krey, T. et al. Crystal structure of the Pestivirus envelope glycoprotein E(rns) and mechanistic analysis of its ribonuclease activity. Structure 20, 862–873 (2012).
pubmed: 22579253
doi: 10.1016/j.str.2012.03.018
Dong, X. et al. A novel virus of Flaviviridae associated with sexual precocity in Macrobrachium rosenbergii. mSystems 6, e0000321 (2021).
pubmed: 34100644
doi: 10.1128/mSystems.00003-21
Sievers, F. et al. Fast, scalable generation of high‐quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol. 7, 539 (2011).
pubmed: 21988835
pmcid: 3261699
doi: 10.1038/msb.2011.75
Capella-Gutiérrez, S., Silla-Martínez, J. M. & Gabaldón, T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25, 1972–1973 (2009).
pubmed: 19505945
pmcid: 2712344
doi: 10.1093/bioinformatics/btp348
Minh, B. Q. et al. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol. Biol. Evol. 37, 1530–1534 (2020).
pubmed: 32011700
pmcid: 7182206
doi: 10.1093/molbev/msaa015
Kalyaanamoorthy, S., Minh, B. Q., Wong, T. K. F., Von Haeseler, A. & Jermiin, L. S. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat. Methods 14, 587–589 (2017).
pubmed: 28481363
pmcid: 5453245
doi: 10.1038/nmeth.4285
Le, T. K. & Vinh, L. S. FLAVI: an amino acid substitution model for flaviviruses. J. Mol. Evol. 88, 445–452 (2020).
pubmed: 32356020
doi: 10.1007/s00239-020-09943-3
Guindon, S. et al. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 59, 307–321 (2010).
pubmed: 20525638
doi: 10.1093/sysbio/syq010
Hoang, D. T., Chernomor, O., von Haeseler, A., Minh, B. Q. & Vinh, L. S. UFBoot2: improving the ultrafast bootstrap approximation. Mol. Biol. Evol. 35, 518–522 (2017).
pmcid: 5850222
doi: 10.1093/molbev/msx281
Paradis, E. & Schliep, K. ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35, 526–528 (2018).
doi: 10.1093/bioinformatics/bty633
Revell, L. J. phytools 2.0: An updated R ecosystem for phylogenetic comparative methods (and other things). PeerJ 12, e16505 (2024).
pubmed: 38192598
pmcid: 10773453
doi: 10.7717/peerj.16505
Yu, G., Smith, D. K., Zhu, H., Guan, Y. & Lam, T. T. ggtree: an R package for visualization and annotation of phylogenetic trees with their covariates and other associated data. Methods Ecol. Evol. 8, 28–36 (2017).
doi: 10.1111/2041-210X.12628
Hackl, T., Ankenbrand, M. & van Adrichem, B. gggenomes: A grammar of graphics for comparative genomics. Github https://github.com/thackl/gggenomes (2024).
Winter, D. J. Rentrez: an R package for the NCBI eUtils API. R J. 9, 520–526 (2017).
doi: 10.32614/RJ-2017-058
Chamberlain, S. A. & Szöcs, E. taxize: taxonomic search and retrieval in R. F1000Res. 2, 191 (2013).
pubmed: 24555091
pmcid: 3901538
doi: 10.12688/f1000research.2-191.v1
Rambaut, A. & Drummond, A. J. FigTree: Tree figure drawing tool, version 1.4.0. http://tree.bio.ed.ac.uk/software/figtree/ (2012).
Jombart, T., Kendall, M., Almagro‐Garcia, J. & Colijn, C. treespace: Statistical exploration of landscapes of phylogenetic trees. Mol. Ecol. Resour. 17, 1385–1392 (2017).
pubmed: 28374552
pmcid: 5724650
doi: 10.1111/1755-0998.12676
Kendall, M. & Colijn, C. Mapping phylogenetic trees to reveal distinct patterns of evolution. Mol. Biol. Evol. 33, 2735–2743 (2016).
pubmed: 27343287
pmcid: 5026250
doi: 10.1093/molbev/msw124
Legendre, P. & Legendre, L. Numerical Ecology (Elsevier, 2012).
Saberi, A., Gulyaeva, A. A., Brubacher, J. L., Newmark, P. A. & Gorbalenya, A. E. A planarian nidovirus expands the limits of RNA genome size. PLoS Pathog. 14, e1007314 (2018).
pubmed: 30383829
pmcid: 6211748
doi: 10.1371/journal.ppat.1007314
Rolland, C., La Scola, B. & Levasseur, A. How Tupanvirus degrades the ribosomal RNA of its amoebal host? The ribonuclease T2 track. Front. Microbiol. 11, 1691 (2020).
pubmed: 32849355
pmcid: 7399046
doi: 10.3389/fmicb.2020.01691
Barrio-Hernandez, I. et al. Clustering predicted structures at the scale of the known protein universe. Nature 622, 637–645 (2023).
pubmed: 37704730
pmcid: 10584675
doi: 10.1038/s41586-023-06510-w
Steinegger, M. & Söding, J. MMseqs2 enables sensitive protein sequence searching for the analysis of massive data sets. Nat. Biotechnol. 35, 1026–1028 (2017).
pubmed: 29035372
doi: 10.1038/nbt.3988
Potter, S. C. et al. HMMER web server: 2018 update. Nucleic Acids Res. 46, 200–204 (2018).
doi: 10.1093/nar/gky448
Gabler, F. et al. Protein sequence analysis using the MPI bioinformatics toolkit. Curr. Protoc. Bioinformatics 72, e108 (2020).
pubmed: 33315308
doi: 10.1002/cpbi.108
Zimmermann, L. et al. A completely reimplemented MPI bioinformatics toolkit with a new HHpred server at its core. J. Mol. Biol. 430, 2237–2243 (2018).
pubmed: 29258817
doi: 10.1016/j.jmb.2017.12.007
Mirdita, M. et al. Uniclust databases of clustered and deeply annotated protein sequences and alignments. Nucleic Acids Res. 45, 170–176 (2017).
doi: 10.1093/nar/gkw1081
Steinegger, M. et al. HH-suite3 for fast remote homology detection and deep protein annotation. BMC Bioinformatics 20, 473 (2019).
pubmed: 31521110
pmcid: 6744700
doi: 10.1186/s12859-019-3019-7
Buchfink, B., Ashkenazy, H., Reuter, K., Kennedy, J. A. & Drost, H.-G. Sensitive clustering of protein sequences at tree-of-life scale using DIAMOND DeepClust. Preprint at bioRxiv https://doi.org/10.1101/2023.01.24.525373 (2023).
Deorowicz, S., Debudaj-Grabysz, A. & Gudyś, A. FAMSA: fast and accurate multiple sequence alignment of huge protein families. Sci. Rep. 6, 33964 (2016).
pubmed: 27670777
pmcid: 5037421
doi: 10.1038/srep33964
Chernomor, O., von Haeseler, A. & Minh, B. Q. Terrace aware data structure for phylogenomic inference from supermatrices. Syst. Biol. 65, 997–1008 (2016).
pubmed: 27121966
pmcid: 5066062
doi: 10.1093/sysbio/syw037
Moi, D. et al. Structural phylogenetics unravels the evolutionary diversification of communication systems in Gram-positive bacteria and their viruses. Preprint at bioRxiv https://doi.org/10.1101/2023.09.19.558401 (2023).