Section: Evolutionary Biology
Topic: Evolution, Genetics/Genomics

Host-symbiont-gene phylogenetic reconciliation

10.24072/pcjournal.273 - Peer Community Journal, Volume 3 (2023), article no. e47.

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Motivation Biological systems are made of entities organized at different scales (e.g. macro-organisms, symbionts, genes…) which evolve in interaction. These interactions range from independence or conflict to cooperation and coevolution, which results in them having a common history. The evolution of such systems is approached by phylogenetic reconciliation, which describes the common patterns of diversification between two different levels, e.g. genes and species, or hosts and symbionts for example. The limit to two levels hides the multi-level inter-dependencies that characterize complex systems. Results We present a probabilistic model of evolution of three nested levels of organization which can account for the codivergence of hosts, symbionts and their genes. This model allows gene transfer as well as host switch, gene duplication as well as symbiont diversification inside a host, gene or symbiont loss. It handles the possibility of ghost lineages as well as temporary free-living symbionts. Given three phylogenetic trees, we devise a Monte Carlo algorithm which samples evolutionary scenarios of symbionts and genes according to an approximation of their likelihood in the model. We evaluate the capacity of our method on simulated data, notably its capacity to infer horizontal gene transfers, and its ability to detect hostsymbiont co-evolution by comparing host/symbiont/gene and symbiont/gene models based on their estimated likelihoods. Then we show in a aphid enterobacter system that some reliable transfers detected by our method, are invisible to classic 2-level reconciliation. We finally evaluate different hypotheses on human population histories in the light of their coevolving Helicobacter pylori symbionts, reconciled together with their genes. Availability Implementation is available on GitHub https://github.com/hmenet/TALE. Data are available on Zenodo https://doi.org/10.5281/zenodo.7667342.

Published online:
DOI: 10.24072/pcjournal.273
Type: Research article
Keywords: symbiont ; holobiont ; phylogeny; evolution ; co-evolution ; horizontal transfer ; host switch ; Helicobacter pylori ; human migrations ; phylogenetic reconciliation
Menet, Hugo 1; Trung, Alexia Nguyen 1; Daubin, Vincent 1; Tannier, Eric 1, 2

1 Univ Lyon, Université Lyon 1, CNRS, Laboratoire de Biométrie et Biologie Évolutive UMR5558, F-69622 Villeurbanne, France
2 Inria, Centre de recherche de Lyon, 69622 Villeurbanne, France
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights
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Menet, Hugo; Trung, Alexia Nguyen; Daubin, Vincent; Tannier, Eric. Host-symbiont-gene phylogenetic reconciliation. Peer Community Journal, Volume 3 (2023), article  no. e47. doi : 10.24072/pcjournal.273. https://peercommunityjournal.org/articles/10.24072/pcjournal.273/

Peer reviewed and recommended by PCI : 10.24072/pci.evolbiol.100593

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

[1] Achtman, M. How old are bacterial pathogens?, Proceedings of the Royal Society B: Biological Sciences, Volume 283 (2016) no. 1836 | DOI

[2] Achtman, M.; Azuma, T.; Berg, D. E.; Ito, Y.; Morelli, G.; Pan, Z.-J.; Suerbaum, S.; Thompson, S. A.; van der Ende, A.; van Doorn, L.-J. Recombination and clonal groupings within Helicobacter pylori from different geographical regions, Molecular Microbiology, Volume 32 (1999) no. 3, pp. 459-470 | DOI

[3] Alberdi, A.; Andersen, S. B.; Limborg, M. T.; Dunn, R. R.; Gilbert, M. T. P. Disentangling host–microbiota complexity through hologenomics, Nature Reviews Genetics, Volume 23 (2021) no. 5, pp. 281-297 | DOI

[4] Anselmetti, Y.; El-Mabrouk, N.; Lafond, M.; Ouangraoua, A. Gene tree and species tree reconciliation with endosymbiotic gene transfer, Bioinformatics, Volume 37 (2021) no. Supplement_1 | DOI

[5] Bailly-Bechet, M.; Martins-Simões, P.; Szöllősi, G. J.; Mialdea, G.; Sagot, M.-F.; Charlat, S. How Long Does Wolbachia Remain on Board?, Molecular Biology and Evolution, Volume 34 (2017) no. 5, pp. 1183-1193 | DOI

[6] Bansal, M. S.; Alm, E. J.; Kellis, M. Efficient algorithms for the reconciliation problem with gene duplication, horizontal transfer and loss, Bioinformatics, Volume 28 (2012) no. 12 | DOI

[7] Bansal, M. S.; Banay, G.; Gogarten, J. P.; Shamir, R. Detecting Highways of Horizontal Gene Transfer, Journal of Computational Biology, Volume 18 (2011) no. 9, pp. 1087-1114 | DOI

[8] Bansal, M. S.; Wu, Y.-C.; Alm, E. J.; Kellis, M. Improved gene tree error correction in the presence of horizontal gene transfer, Bioinformatics, Volume 31 (2015) no. 8, pp. 1211-1218 | DOI

[9] Boussau, B.; Scornavacca, C. Reconciling Gene trees with Species Trees In: In: Phylogenetics in the Genomic Era. Ed. by Celine Scornavacca , Frédéric Delsuc, and Nicolas Galtier (2020) (https://hal.archives-ouvertes.fr/hal-02535529)

[10] Charleston, M.; Libeskind-Hadas, R. Event-Based Cophylogenetic Comparative Analysis, Modern Phylogenetic Comparative Methods and Their Application in Evolutionary Biology, Springer Berlin Heidelberg, Berlin, Heidelberg, 2014, pp. 465-480 | DOI

[11] Chauve, C.; Rafiey, A.; Davín, A. A.; Scornavacca, C.; Veber, P.; Boussau, B.; Szöllősi, G. J.; Daubin, V.; Tannier, E. MaxTiC: Fast ranking of a phylogenetic tree by Maximum Time Consistency with lateral gene transfers, bioRxiv, 2017 | DOI

[12] David, L. A.; Alm, E. J. Rapid evolutionary innovation during an Archaean genetic expansion, Nature, Volume 469 (2010) no. 7328, pp. 93-96 | DOI

[13] Davín, A. A.; Tannier, E.; Williams, T. A.; Boussau, B.; Daubin, V.; Szöllősi, G. J. Gene transfers can date the tree of life, Nature Ecology & Evolution, Volume 2 (2018) no. 5, pp. 904-909 | DOI

[14] Donati, B.; Baudet, C.; Sinaimeri, B.; Crescenzi, P.; Sagot, M.-F. EUCALYPT: efficient tree reconciliation enumerator, Algorithms for Molecular Biology, Volume 10 (2015) no. 1 | DOI

[15] Doyon, J.-P.; Ranwez, V.; Daubin, V.; Berry, V. Models, algorithms and programs for phylogeny reconciliation, Briefings in Bioinformatics, Volume 12 (2011) no. 5, pp. 392-400 | DOI

[16] Duchemin, W.; Anselmetti, Y.; Patterson, M.; Ponty, Y.; B�rard, S.; Chauve, C.; Scornavacca, C.; Daubin, V.; Tannier, E. DeCoSTAR: Reconstructing the Ancestral Organization of Genes or Genomes Using Reconciled Phylogenies, Genome Biology and Evolution, Volume 9 (2017) no. 5, pp. 1312-1319 | DOI

[17] Duchemin, W.; Daubin, V.; Tannier, E. Reconstruction of an ancestral Yersinia pestisgenome and comparison with an ancient sequence, BMC Genomics, Volume 16 (2015) no. S10 | DOI

[18] Duchemin, W.; Gence, G.; Arigon Chifolleau, A.-M.; Arvestad, L.; Bansal, M. S.; Berry, V.; Boussau, B.; Chevenet, F.; Comte, N.; Davín, A. A.; Dessimoz, C.; Dylus, D.; Hasic, D.; Mallo, D.; Planel, R.; Posada, D.; Scornavacca, C.; Szöllősi, G.; Zhang, L.; Tannier, É.; Daubin, V. RecPhyloXML: a format for reconciled gene trees, Bioinformatics, Volume 34 (2018) no. 21, pp. 3646-3652 | DOI

[19] Felsenstein, J. Inferring Phylogenies, Oxford University Press, Oxford, New York, 2003, 580 pages

[20] Fournier, G. P.; Huang, J.; Gogarten, J. P. Horizontal gene transfer from extinct and extant lineages: biological innovation and the coral of life, Philosophical Transactions of the Royal Society B: Biological Sciences, Volume 364 (2009) no. 1527, pp. 2229-2239 | DOI

[21] Jacox, E.; Chauve, C.; Szöllősi, G. J.; Ponty, Y.; Scornavacca, C. ecceTERA: comprehensive gene tree-species tree reconciliation using parsimony, Bioinformatics, Volume 32 (2016) no. 13, pp. 2056-2058 | DOI

[22] Jolley, K. A.; Bray, J. E.; Maiden, M. C. J. Open-access bacterial population genomics: BIGSdb software, the PubMLST.org website and their applications, Wellcome Open Research, Volume 3 (2018) | DOI

[23] Jousselin, E. Reconciling molecular evolution and evolutionary ecology studies: a phylogenetic reconciliation method for gene-symbiont-host systems, Peer Community in Evolutionary Biology (2023) | DOI

[24] Kordi, M.; Kundu, S.; Bansal, M. S. On Inferring Additive and Replacing Horizontal Gene Transfers Through Phylogenetic Reconciliation, Proceedings of the 10th ACM International Conference on Bioinformatics, Computational Biology and Health Informatics (2019) | DOI

[25] Kundu, S.; Bansal, M. S. SaGePhy: an improved phylogenetic simulation framework for gene and subgene evolution, Bioinformatics, Volume 35 (2019) no. 18, pp. 3496-3498 | DOI

[26] Li, L.; Bansal, M. S. An Integer Linear Programming Solution for the Domain-Gene-Species Reconciliation Problem, Proceedings of the 2018 ACM International Conference on Bioinformatics, Computational Biology, and Health Informatics (2018) | DOI

[27] Li, L.; Bansal, M. S. An Integrated Reconciliation Framework for Domain, Gene, and Species Level Evolution, IEEE/ACM Transactions on Computational Biology and Bioinformatics, Volume 16 (2019) no. 1, pp. 63-76 | DOI

[28] Li, L.; Bansal, M. S. Simultaneous Multi-Domain-Multi-Gene Reconciliation Under the Domain-Gene-Species Reconciliation Model, Bioinformatics Research and Applications, Springer International Publishing, Cham, 2019, pp. 73-86 | DOI

[29] Manzano-Marı́n, A.; Coeur d’acier, A.; Clamens, A.-L.; Orvain, C.; Cruaud, C.; Barbe, V.; Jousselin, E. Serial horizontal transfer of vitamin-biosynthetic genes enables the establishment of new nutritional symbionts in aphids’ di-symbiotic systems, The ISME Journal, Volume 14 (2019) no. 1, pp. 259-273 | DOI

[30] Martínez-Aquino, A. Phylogenetic framework for coevolutionary studies: a compass for exploring jungles of tangled trees, Current Zoology, Volume 62 (2016) no. 4, pp. 393-403 | DOI

[31] Mégraud, F.; Lehours, P.; Vale, F. The history of Helicobacter pylori : from phylogeography to paleomicrobiology, Clinical Microbiology and Infection, Volume 22 (2016) no. 11, pp. 922-927 | DOI

[32] Menardo, F.; Loiseau, C.; Brites, D.; Coscolla, M.; Gygli, S. M.; Rutaihwa, L. K.; Trauner, A.; Beisel, C.; Borrell, S.; Gagneux, S. Treemmer: a tool to reduce large phylogenetic datasets with minimal loss of diversity, BMC Bioinformatics, Volume 19 (2018) no. 1 | DOI

[33] Mendler, K.; Chen, H.; Parks, D. H.; Lobb, B.; Hug, L. A.; Doxey, A. C. AnnoTree: visualization and exploration of a functionally annotated microbial tree of life, Nucleic Acids Research, Volume 47 (2019) no. 9, pp. 4442-4448 | DOI

[34] Menet, H.; Daubin, V.; Tannier, E. Phylogenetic reconciliation, PLOS Computational Biology, Volume 18 (2022) no. 11 | DOI

[35] Menet, H.; Nguyen Trung, A.; Daubin, V.; Tannier, E. Host symbiont gene reconciliation supple- mentary material [Data set], Zenodo, 2023 | DOI

[36] Morel, B.; Kozlov, A. M.; Stamatakis, A.; Szöllősi, G. J. GeneRax: A Tool for Species-Tree-Aware Maximum Likelihood-Based Gene  Family Tree Inference under Gene Duplication, Transfer, and Loss, Molecular Biology and Evolution, Volume 37 (2020) no. 9, pp. 2763-2774 | DOI

[37] Morel, B.; Schade, P.; Lutteropp, S.; Williams, T. A.; Szöllősi, G. J.; Stamatakis, A. SpeciesRax: A Tool for Maximum Likelihood Species Tree Inference from Gene Family Trees under Duplication, Transfer, and Loss, Molecular Biology and Evolution, Volume 39 (2022) no. 2 | DOI

[38] Muhammad, S. A.; Sennblad, B.; Lagergren, J. Species tree-aware simultaneous reconstruction of gene and domain evolution, bioRxiv, 2018 | DOI

[39] Mykowiecka, A.; Muszewska, A.; Gorecki, P. Inferring time-consistent and well-supported horizontal gene transfers, 2018 IEEE International Conference on Bioinformatics and Biomedicine (BIBM) (2018) | DOI

[40] Nakabachi, A.; Ueoka, R.; Oshima, K.; Teta, R.; Mangoni, A.; Gurgui, M.; Oldham, N. J.; van Echten-Deckert, G.; Okamura, K.; Yamamoto, K.; Inoue, H.; Ohkuma, M.; Hongoh, Y.; Miyagishima, S.-y.; Hattori, M.; Piel, J.; Fukatsu, T. Defensive Bacteriome Symbiont with a Drastically Reduced Genome, Current Biology, Volume 23 (2013) no. 15, pp. 1478-1484 | DOI

[41] Nakhleh, L. Computational approaches to species phylogeny inference and gene tree reconciliation, Trends in Ecology & Evolution, Volume 28 (2013) no. 12, pp. 719-728 | DOI

[42] Nikoh, N.; Hosokawa, T.; Moriyama, M.; Oshima, K.; Hattori, M.; Fukatsu, T. Evolutionary origin of insect–Wolbachia nutritional mutualism, Proceedings of the National Academy of Sciences, Volume 111 (2014) no. 28, pp. 10257-10262 | DOI

[43] Penel, S.; Menet, H.; Tricou, T.; Daubin, V.; Tannier, E. Thirdkind: displaying phylogenetic encounters beyond 2-level reconciliation, Bioinformatics, Volume 38 (2022) no. 8, pp. 2350-2352 | DOI

[44] Penz, T.; Schmitz-Esser, S.; Kelly, S. E.; Cass, B. N.; Müller, A.; Woyke, T.; Malfatti, S. A.; Hunter, M. S.; Horn, M. Comparative Genomics Suggests an Independent Origin of Cytoplasmic Incompatibility in Cardinium hertigii, PLoS Genetics, Volume 8 (2012) no. 10 | DOI

[45] Rasmussen, M. D.; Kellis, M. Unified modeling of gene duplication, loss, and coalescence using a locus tree, Genome Research, Volume 22 (2012) no. 4, pp. 755-765 | DOI

[46] Ravenhall, M.; Škunca, N.; Lassalle, F.; Dessimoz, C. Inferring Horizontal Gene Transfer, PLOS Computational Biology, Volume 11 (2015) no. 5 | DOI

[47] Ree, R. H.; Moore, B. R.; Webb, C. O.; Donoghue, M. J. A likelihood framework for inferring the evolution of geographic range on phylogenetic trees, Evolution, Volume 59 (2005) no. 11, pp. 2299-2311 | DOI

[48] Ree, R. H.; Smith, S. A. Maximum Likelihood Inference of Geographic Range Evolution by Dispersal, Local Extinction, and Cladogenesis, Systematic Biology, Volume 57 (2008) no. 1, pp. 4-14 | DOI

[49] Ronquist, F. Dispersal-Vicariance Analysis: A New Approach to the Quantification of Historical Biogeography, Systematic Biology, Volume 46 (1997) no. 1, pp. 195-203 | DOI

[50] Santichaivekin, S.; Yang, Q.; Liu, J.; Mawhorter, R.; Jiang, J.; Wesley, T.; Wu, Y.-C.; Libeskind-Hadas, R. eMPRess: a systematic cophylogeny reconciliation tool, Bioinformatics, Volume 37 (2020) no. 16, pp. 2481-2482 | DOI

[51] Sapp, J. Evolution by association, Oxford University Press, Oxford, UK, 1994

[52] Sjostrand, J.; Tofigh, A.; Daubin, V.; Arvestad, L.; Sennblad, B.; Lagergren, J. A Bayesian Method for Analyzing Lateral Gene Transfer, Systematic Biology, Volume 63 (2014) no. 3, pp. 409-420 | DOI

[53] Sonnenburg, J. L.; Sonnenburg, E. D. Vulnerability of the industrialized microbiota, Science, Volume 366 (2019) no. 6464 | DOI

[54] Stolzer, M.; Siewert, K.; Lai, H.; Xu, M.; Durand, D. Event inference in multidomain families with phylogenetic reconciliation, BMC Bioinformatics, Volume 16 (2015) no. S14 | DOI

[55] Szöllősi, G. J.; Tannier, E.; Lartillot, N.; Daubin, V. Lateral Gene Transfer from the Dead, Systematic Biology, Volume 62 (2013) no. 3, pp. 386-397 | DOI

[56] Szöllősi, G. J.; Boussau, B.; Abby, S. S.; Tannier, E.; Daubin, V. Phylogenetic modeling of lateral gene transfer reconstructs the pattern and relative timing of speciations, Proceedings of the National Academy of Sciences, Volume 109 (2012) no. 43, pp. 17513-17518 | DOI

[57] Szöllősi, G. J.; Davín, A. A.; Tannier, E.; Daubin, V.; Boussau, B. Genome-scale phylogenetic analysis finds extensive gene transfer among fungi, Philosophical Transactions of the Royal Society B: Biological Sciences, Volume 370 (2015) no. 1678 | DOI

[58] Szöllősi, G. J.; Rosikiewicz, W.; Boussau, B.; Tannier, E.; Daubin, V. Efficient Exploration of the Space of Reconciled Gene Trees, Systematic Biology, Volume 62 (2013) no. 6, pp. 901-912 | DOI

[59] Szöllősi, G. J.; Tannier, E.; Daubin, V.; Boussau, B. The Inference of Gene Trees with Species Trees, Systematic Biology, Volume 64 (2014) no. 1 | DOI

[60] Tricou, T.; Tannier, E.; de Vienne, D. M. Ghost lineages can invalidate or even reverse findings regarding gene flow, PLOS Biology, Volume 20 (2022) no. 9 | DOI

[61] Waskito, L. A.; Yamaoka, Y. The Story of Helicobacter pylori: Depicting Human Migrations from the Phylogeography, Advances in Experimental Medicine and Biology, Springer International Publishing, Cham, 2019, pp. 1-16 | DOI

[62] Wieseke, N.; Hartmann, T.; Bernt, M.; Middendorf, M. Cophylogenetic Reconciliation with ILP, IEEE/ACM Transactions on Computational Biology and Bioinformatics, Volume 12 (2015) no. 6, pp. 1227-1235 | DOI

[63] Wijayawardena, B. K.; Minchella, D. J.; DeWoody, J. A. Hosts, parasites, and horizontal gene transfer, Trends in Parasitology, Volume 29 (2013) no. 7, pp. 329-338 | DOI

[64] Yang, Z. Computational molecular evolution, Oxford series in ecology and evolution, Oxford University Press, Oxford, UK, 2006

[65] Zhaxybayeva, O.; Peter Gogarten, J. Cladogenesis, coalescence and the evolution of the three domains of life, Trends in Genetics, Volume 20 (2004) no. 4, pp. 182-187 | DOI

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