Exploring syntenic conservation across genomes for phylogenetic studies of organisms subjected to horizontal gene transfers: a case study with Cyanobacteria and cyanolichens

Cornet, Luc; Magain, Nicolas; Baurain, Denis; Lutzoni, François

doi:10.1016/j.ympev.2021.107100

Article (Scientific journals)

Exploring syntenic conservation across genomes for phylogenetic studies of organisms subjected to horizontal gene transfers: a case study with Cyanobacteria and cyanolichens

Cornet, Luc; Magain, Nicolas; Baurain, Denis et al.

2021 • In Molecular Phylogenetics and Evolution

Peer Reviewed verified by ORBi

Permalink
https://hdl.handle.net/2268/257946

DOI
10.1016/j.ympev.2021.107100

PubMed
33592234

Files (1)Send to Details Statistics Bibliography Similar publications

Files

Full Text

MPE-D-20-00380_R1.pdf

Author preprint (4.11 MB)

Request a copy

All documents in ORBi are protected by a user license.

Send to

RIS BibTex APA Chicago Permalink X Linkedin

Details

Keywords :

Lichens; Cyanobacteria; Horizontal Gene Transfers

Abstract :

[en] Understanding the evolutionary history of symbiotic Cyanobacteria at a fine scale is essential to unveil patterns of associations with their hosts and factors driving their spatiotemporal interactions. As for bacteria in general, Horizontal Gene Transfers (HGT) are expected to be rampant throughout their evolution, which justified the use of single-locus phylogenies in macroevolutionary studies of these photoautotrophic bacteria. Genomic approaches have greatly increased the amount of molecular data available, but the selection of orthologous, congruent genes that are more likely to reflect bacterial macroevolutionary histories remains problematic. In this study, we developed a synteny-based approach and searched for Collinear Orthologous Regions (COR), under the assumption that genes that are present in the same order and orientation across a wide monophyletic clade are less likely to have undergone HGT. We searched sixteen reference Nostocales genomes and identified 99 genes, part of 28 COR comprising three to eight genes each. We then developed a bioinformatic pipeline, designed to minimize inter-genome contamination and processed twelve Nostoc-associated lichen metagenomes. This reduced our original dataset to 90 genes representing 25 COR, which were used to infer phylogenetic relationships within Nostocales and among lichenized Cyanobacteria. This dataset was narrowed down further to 71 genes representing 22 COR by selecting only genes part of one (largest) operon per COR. We found a relatively high level of congruence among trees derived from the 90-gene dataset, but congruence was only slightly higher among genes within a COR compared to genes across COR. However, topological congruence was significantly higher among the 71 genes part of one operon per COR. Nostocales phylogenies resulting from concatenation and species tree approaches based on the 90- and 71-gene datasets were highly congruent, but the most highly supported result was obtained when using synteny, collinearity, and operon information (i.e., 71-gene dataset) as gene selection criteria, which outperformed larger datasets with more genes.

Disciplines :

Microbiology

Author, co-author :

Cornet, Luc ; Université de Liège - ULiège > Département des sciences de la vie > Phylogénomique des eucaryotes

Magain, Nicolas ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Biologie de l'évolution et gestion de la biodiversité

Baurain, Denis ; Université de Liège - ULiège > Département des sciences de la vie > Phylogénomique des eucaryotes

Lutzoni, François; Duke University

Language :

English

Title :

Exploring syntenic conservation across genomes for phylogenetic studies of organisms subjected to horizontal gene transfers: a case study with Cyanobacteria and cyanolichens

Publication date :

14 February 2021

Journal title :

Molecular Phylogenetics and Evolution

ISSN :

1055-7903

eISSN :

1095-9513

Publisher :

Elsevier, Atlanta, United States - California

Peer reviewed :

Peer Reviewed verified by ORBi

Tags :

CÉCI : Consortium des Équipements de Calcul Intensif

Funders :

F.R.S.-FNRS - Fonds de la Recherche Scientifique
NSF - National Science Foundation
BELSPO - Service Public Fédéral de Programmation Politique scientifique
FRIA - Fonds pour la Formation à la Recherche dans l'Industrie et dans l'Agriculture
ULiège - Université de Liège
FWB - Fédération Wallonie-Bruxelles

Funding number :

National Science Foundation (DEB‐1025930 and DEB‐1556995)

Available on ORBi :

since 13 March 2021

Statistics

Number of views

122 (26 by ULiège)

Number of downloads

7 (4 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

OpenAlex citations

Bibliography

Abby, S.S., Tannier, E., Gouy, M., Daubin, V., Lateral gene transfer as a support for the tree of life. Proc. Natl. Acad. Sci. 109 (2012), 4962–4967.
Arnold, A.E., Miadlikowska, J., Higgins, K.L., Sarvate, S.D., Gugger, P., Way, A., Hofstetter, V., Kauff, F., Lutzoni, F., A phylogenetic estimation of trophic transition networks for ascomycetous fungi: Are lichens cradles of symbiotrophic fungal diversification?. Syst. Biol. 58 (2009), 283–297.
Armaleo, D., May, S., Sizing the fungal and algal genomes of the lichen Cladonia grayi through quantitative PCR. Symbiosis 49 (2009), 43–51.
Armaleo, D., Müller, O., Lutzoni, F., Andrésson, Ó.S., Blanc, G., Bode, H.B., Collart, F.R., DalGrande, F., Dietrich, F., Grigoriev, I.V., Joneson, S., Kuo, A., Larsen, P.E., Logsdon, J.M., Lopez, D., Martin, F., May, S.P., McDonald, T.R., Merchant, S.S., Miao, V., Morin, E., Oono, R., Pellegrini, M., Rubinstein, N., Sanchez-Puerta, M.V., Savelkoul, E., Schmitt, I., Slot, J.C., Soanes, D., Szoevenyi, P., Talbot, N.J., Veneault-Fourrey, C., Xavier, B.B., The lichen symbiosis re-viewed through the genomes of Cladonia grayi and its algal partner Asterochloris glomerata. BMC Genomics, 20, 2019, 605.
Aschenbrenner, I.A., Cernava, T., Berg, G., Grube, M., Understanding microbial multi-species symbioses. Front. Microbiol., 7, 2016, 180.
Bell-Doyon, P., Laroche, J., Saltonstall, K., Villarreal Aguilar, J.C., Specialized bacteriome uncovered in the coralloid roots of the epiphytic gymnosperm, Zamia pseudoparasitica. Environ. DNA, 2020.
Bi, G., Mao, Y., Xing, Q., Cao, M., HomBlocks: A multiple-alignment construction pipeline for organelle phylogenomics based on locally collinear block searching. Genomics 110 (2018), 18–22.
Boekels-Gogarten, M., Gogarten, J.P., Olendzenski, L., (eds.) Horizontal gene transfer: genomes in flux, 2009, Humana Press, New York, 500.
Bolger, A.M., Lohse, M., Usadel, B., Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30 (2014), 2114–2120.
Brown, N.M., Mueller, R.S., Shepardson, J.W., Landry, Z.C., Morré, J.T., Maier, C.S., Hardy, J., Dreher, T.W., Structural and functional analysis of the finished genome of the recently isolated toxic Anabaena sp. WA102. BMC Genomics, 17(1), 2016, 457.
Buchfink, B., Xie, C., Huson, D.H., Fast and sensitive protein alignment using DIAMOND. Nat. Methods 12 (2015), 59–60.
Casano, L.M., del Campo, E.M., García-Breijo, F.J., Reig-Armiñana, J., Gasulla, F., Del Hoyo, A., Guéra, A., Barreno, E., Two Trebouxia algae with different physiological performances are ever-present in lichen thalli of Ramalina farinacea. Coexistence versus Competition?. Environ. Microbiol. 13 (2011), 806–818.
Contreras-Moreira, B., Vinuesa, P., GET_HOMOLOGUES, a versatile software package for scalable and robust microbial pangenome analysis. Appl. Environ. Microbiol. 79 (2013), 7696–7701.
Cornet, L., Meunier, L., Vlierberghe, M.V., Léonard, R.R., Durieu, B., Lara, Y., Misztak, A., Sirjacobs, D., Javaux, E.J., Philippe, H., et al. Consensus assessment of the contamination level of publicly available cyanobacterial genomes. PLoS ONE, 13, 2018, e0200323.
Cornet, L., Wilmotte, A., Javaux, E.J., Baurain, D., A constrained SSU-rRNA phylogeny reveals the unsequenced diversity of photosynthetic Cyanobacteria (Oxyphotobacteria). BMC Res. Notes, 11, 2018, 435.
Criscuolo, A., Gribaldo, S., BMGE (Block Mapping and Gathering with Entropy): a new software for selection of phylogenetic informative regions from multiple sequence alignments. BMC Evol Biol, 10, 2010, 210.
Cubero, O.F., Crespo, A.N.A., Fatehi, J., Bridge, P.D., DNA extraction and PCR amplification method suitable for fresh, herbarium-stored, lichenized, and other fungi. Plant Syst. Evol. 216:3 (1999), 243–249.
Dal Forno, M., Lawrey, J.D., Sikaroodi, M., Gillevet, P.M., Schuettpelz, E., Lücking, R., Extensive photobiont sharing in a rapidly radiating cyanolichen clade. Mol. Ecol., 2020, 10.1111/mec.15700.
Dal Grande, F., Rolshausen, G., Divakar, P.K., Crespo, A., Otte, J., Schleuning, M., Schmitt, I., Environment and host identity structure communities of green algal symbionts in lichens. New Phytol. 217:1 (2017), 277–289.
Darriba, D., Taboada, G.L., Doallo, R., Posada, D., ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 27:8 (2011), 1164–1165.
Delsuc, F., Brinkmann, H., Philippe, H., Phylogenomics and the reconstruction of the tree of life. Nat. Rev. Genet. 6 (2005), 361–375.
Doolittle, W.F., Phylogenetic classification and the universal tree. Science 284:5423 (1999), 2124–2128.
Drillon, G., Carbone, A., Fischer, G., SynChro: a fast and easy tool to reconstruct and visualize synteny blocks along eukaryotic chromosomes. PLoS ONE, 9, 2014, e92621.
Edgar, R.C., Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26 (2010), 2460–2461.
Elvebakk, A., Papaefthimiou, D., Robertsen, E.H., Liaimer, A., Phylogenetic patterns among Nostoc cyanobionts within bi- and tripartite lichens of the genus Pannaria. J. Phycol. 44:4 (2008), 1049–1059.
Emms, D.M., Kelly, S., OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biol., 16, 2015, 157.
Fedrowitz, K., Kaasalainen, U., Rikkinen, J., Genotype variability of Nostoc symbionts associated with three epiphytic Nephroma species in a boreal forest landscape. The Bryologist 114:1 (2011), 220–230.
Friedl, T., Büdel, B., Photobionts. Nash, T.H., (eds.) Lichen Biology, 2008, Cambridge University Press, Cambridge, UK, 9–26.
Gribaldo, S., Brochier, C., Phylogeny of prokaryotes: does it exist and why should we care?. Res. Microbiol. 160:7 (2009), 513–521.
Guimarães, P.R. Jr, Jordano, P., Thompson, J.N., Evolution and coevolution in mutualistic networks. Ecol. Lett. 14:9 (2011), 877–885.
Hauer, T., Bohunická, M., Johansen, J.R., Mareš, J., Berrendero-Gomez, E., Reassessment of the cyanobacterial family Microchaetaceae and establishment of new families Tolypothrichaceae and Godleyaceae. J. Phycol. 50:6 (2014), 1089–1100.
Hilario, E., Gogarten, J.P., Horizontal transfer of ATPase genes—the tree of life becomes a net of life. Biosystems 31:2–3 (1993), 111–119.
Hillis, D.M., Bull, J.J., An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Syst. Biol. 42:2 (1993), 182–192.
Hirose, Y., Fujisawa, T., Ohtsubo, Y., Katayama, M., Misawa, N., Wakazuki, S., Shimura, Y., Nakamura, Y., Kawachi, M., Yoshikawa, H., et al. Complete genome sequence of cyanobacterium Fischerella sp. NIES-3754, providing thermoresistant optogenetic tools. J. Biotechnol. 220 (2016), 45–46.
Hirose, Y., Fujisawa, T., Ohtsubo, Y., Katayama, M., Misawa, N., Wakazuki, S., Shimura, Y., Nakamura, Y., Kawachi, M., Yoshikawa, H., et al. Complete genome sequence of cyanobacterium Nostoc sp. NIES-3756, a potentially useful strain for phytochrome-based bioengineering. J. Biotechnol. 218 (2016), 51–52.
Hodkinson, B.P., Gottel, N.R., Schadt, C.W., Lutzoni, F., Photoautotrophic symbiont and geography are major factors affecting highly structured and diverse bacterial communities in the lichen microbiome. Environ. Microbiol. 14:1 (2012), 147–161.
Honegger, R., The symbiotic phenotype of lichen-forming ascomycetes and their endo- and epi-bionts. Fungal associations. second ed., 2012, Springer, Berlin Heidelberg, 165–188.
Hyvärinen, M., Härdling, R., Tuomi, J., Cyanobacterial lichen symbiosis: The fungal partner as an optimal harvester. Oikos 98 (2002), 498–504.
Irisarri, I., Baurain, D., Brinkmann, H., Delsuc, F., Sire, J.-Y., Kupfer, A., Petersen, J., Jarek, M., Meyer, A., Vences, M., Philippe, H., Phylotranscriptomic consolidation of the jawed vertebrate timetree. Nat. Ecol. Evol. 1 (2017), 1370–1378.
Isojärvi, J., Shunmugam, S., Sivonen, K., Allahverdiyeva, Y., Aro, E.M., Battchikova, N., Draft genome sequence of Calothrix strain 336/3, a novel H2-producing cyanobacterium isolated from a Finnish lake. Genome Announcements 3:1 (2015), e01474–e1514.
Jüriado, I., Kaasalainen, U., Jylhä, M., Rikkinen, J., Relationships between mycobiont identity, photobiont specificity and ecological preferences in the lichen genus Peltigera (Ascomycota) in Estonia (northeastern Europe). Fungal Ecol. 39 (2019), 45–54.
Kaasalainen, U., Olsson, S., Rikkinen, J., Evolution of the tRNALeu (UAA) intron and congruence of genetic markers in lichen-symbiotic Nostoc. PLoS ONE, 10(6), 2015, e0131223.
Kang, D.D., Froula, J., Egan, R., Wang, Z., MetaBAT, an efficient tool for accurately reconstring single genomes from complex microbial communities. PeerJ, 3, 2015, e1165.
Katoh, K., Standley, D.M., MAFFT Multiple sequence alignment software Version 7: improvements in performance and usability. Mol. Biol. Evol. 30 (2013), 772–780.
Khan, M.A., Mahmudi, O., Ullah, I., Arvestad, L., Lagergren, J., Probabilistic inference of lateral gene transfer events. BMC Bioinf., 2016(17), 2016, 431.
Kroken, S., Taylor, J.W., Phylogenetic species, reproductive mode, and specificity of the green alga Trebouxia forming lichens with the fungal genus Letharia. The Bryologist 103:4 (2000), 645–660.
Kubatko, L.S., Degnan, J.H., Inconsistency of phylogenetic estimates from concatenated data under coalescence. Syst. Biol. 56:1 (2007), 17–24.
Lanfear, R., Calcott, B., Ho, S.Y.W., Guindon, S., PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol. Biol. Evol. 29 (2012), 1695–1701.
Lanfear, R., Frandsen, P.B., Wright, A.M., Senfeld, T., Calcott, B., PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Mol. Biol. Evol. 34 (2017), 772–773.
Laurin-Lemay, S., Brinkmann, H., Philippe, H., Origin of land plants revisited in the light of sequence contamination and missing data. Curr. Biol. 22 (2012), R593–R594.
Leão, T., Guimarães, P.I., de Melo, A.G.C., Ramos, R.T.J., Leão, P.N., Silva, A., Fiore, M.F., Schneider, M.P.C., Draft genome sequence of the N2-fixing cyanobacterium Nostoc piscinale CENA21, isolated from the Brazilian Amazon floodplain. Genome Announcements 4:2 (2016), e00189–e216.
Lee, J.Z., Burow, L.C., Woebken, D., Everroad, R.C., Kubo, M.D., Spormann, A.M., et al. Fermentation couples Chloroflexi and sulfate-reducing bacteria to Cyanobacteria in hypersaline microbial mats. Front. Microbiol. 2014 (2014), 5–61.
Liu, L., Yu, L., Edwards, S.V., A maximum pseudo-likelihood approach for estimating species trees under the coalescent model. BMC Evol. Biol., 10(1), 2010, 302.
Lohtander, K., Oksanen, I., Rikkinen, J., Genetic diversity of green algal and cyanobacterial photobionts in Nephroma (Peltigerales). The Lichenologist 35:4 (2003), 325–339.
Lutzoni, F., Miadlikowska, J., Lichens. Curr. Biol. 19:13 (2009), R502–R503.
Magain, N., Miadlikowska, J., Goffinet, B., Sérusiaux, E., Lutzoni, F., Macroevolution of specificity in cyanolichens of the genus Peltigera section Polydactylon (Lecanoromycetes, Ascomycota). Syst. Biol. 66:1 (2017), 74–99.
Magain, N., Miadlikowska, J., Mueller, O., Gajdeczka, M., Truong, C., Salamov, A.A., Dubchak, I., Grigoriev, I.V., Goffinet, B., Sérusiaux, E., Lutzoni, F., Conserved genomic collinearity as a source of broadly applicable, fast evolving, markers to resolve species complexes: a case study using the lichen-forming genus Peltigera section Polydactylon. Mol. Phylogenet. Evol. 117 (2017), 10–29.
Magain, N., Sérusiaux, E., Do photobiont switch and cephalodia emancipation act as evolutionary drivers in the lichen symbiosis? A case study in the Pannariaceae (Peltigerales). PLoS ONE, 9(2), 2014, e89876.
Magain, N., Truong, C., Goward, T., Niu, D., Goffinet, B., Sérusiaux, E., Lutzoni, F., Miadlikowska, J., Species delimitation at a global scale reveals high species richness with complex biogeography and patterns of symbiont association in Peltigera section Peltigera (lichenized Ascomycota: Lecanoromycetes). Taxon 67:5 (2018), 836–870.
Manen, J.F., Falquet, J., The cpcB-cpcA locus as a tool for the genetic characterization of the genus Arthrospira (Cyanobacteria): evidence for horizontal transfer. Int. J. Syst. Evol. Microbiol. 52:3 (2002), 861–867.
McDonald, T.R., Mueller, O., Dietrich, F.S., Lutzoni, F., High-throughput genome sequencing of lichenizing fungi to assess gene loss in the ammonium transporter/ammonia permease gene family. BMC Genomics, 14(1), 2013, 225.
Miadlikowska, J., Lutzoni, F., Phylogenetic revision of the genus Peltigera (lichen-forming Ascomycota) based on morphological, chemical, and large subunit nuclear ribosomal DNA data. Int. J. Plant Sci. 161:6 (2000), 925–958.
Miadlikowska, J., Richardson, D., Magain, N., Ball, B., Anderson, F., Cameron, R., Lendemer, J., Truong, C., Lutzoni, F., Phylogenetic placement, species delimitation, and cyanobiont identity of endangered aquatic Peltigera species (lichen-forming Ascomycota, Lecanoromycetes). Am. J. Bot. 101:7 (2014), 1141–1156.
Miller, M.A., Pfeiffer, W., Schwartz, T., 2010. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Gateway Computing Environments Workshop (GCE), 2010, pp. 1–8. IEEE.
Mirarab, S., Warnow, T., ASTRAL-II: coalescent-based species tree estimation with many hundreds of taxa and thousands of genes. Bioinformatics 31:12 (2015), i44–i52.
Muggia, L., Nelsen, M.P., Kirika, P.M., Barreno, E., Beck, A., Lindgren, H., Lumbsch, H.T., Leavitt, S.D., Trebouxia working group, Formally described species woefully underrepresent phylogenetic diversity in the common lichen photobion genus Trebouxia (Trebouxiophyceae, Chlorophyta): an impetus for developing an integrated taxonomy. Mol. Phylogenet. Evol., 149, 2020, 106821.
Myllys, L., Stenroos, S., Thell, A., Kuusinen, M., High cyanobiont selectivity of epiphytic lichens in old growth boreal forest of Finland. New Phytol. 173:3 (2007), 621–629.
Nash, T.H., Lichen Biology. Second Edition, 2008, Cambridge University Press, New York.
Nelson, J.M., Hauser, D.A., Gudiño, J.A., Guadalupe, Y.A., Meeks, J.C., Salazar Allen, N., Villarreal, J.C., Li, F.W., Complete genomes of symbiotic cyanobacteria clarify the evolution of vanadium-nitrogenase. Genome Biol. Evol. 11:7 (2019), 1959–1964.
Nurk, S., Meleshko, D., Korobeynikov, A., Pevzner, P.A., metaSPAdes: a new versatile metagenomic assembler. Genome Res. 27 (2017), 824–834.
O'Brien, H.E., Miadlikowska, J., Lutzoni, F., Assessing host specialization in symbiotic cyanobacteria associated with four closely related species of the lichen fungus Peltigera. Eur. J. Phycol. 40:4 (2005), 363–378.
O'Brien, H.E., Miadlikowska, J., Lutzoni, F., Assessing population structure and host specialization in lichenized cyanobacteria. New Phytol. 198:2 (2013), 557–566.
Onuț-Brännström, I., Benjamin, M., Scofield, D.G., Heiðmarsson, S., Andersson, M.G., Lindström, E.S., Johannesson, H., Sharing of photobionts in sympatric populations of Thamnolia and Cetraria lichens: evidence from high-throughput sequencing. Sci. Rep., 8(1), 2018, 4406.
Otálora, M.A., Martínez, I., O'Brien, H., Molina, M.C., Aragón, G., Lutzoni, F., Multiple origins of high reciprocal symbiotic specificity at an intercontinental spatial scale among gelatinous lichens (Collemataceae, Lecanoromycetes). Mol. Phylogenet. Evol. 56:3 (2010), 1089–1095.
Pardo-De la Hoz, C., Magain, N., Lutzoni, F., Goward, T., Restrepo, S., Miadlikowska, J., Contrasting symbiotic patterns in two closely related lineages of trimembered lichens of the genus Peltigera. Front. Microbiol., 9, 2018, 2770.
Parks, D.H., Imelfort, M., Skennerton, C.T., Hugenholtz, P., Tyson, G.W., CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 25 (2015), 1043–1055.
Paulsrud, P., Rikkinen, J., Lindblad, P., Cyanobiont specificity in some Nostoc-containing lichens and in a Peltigera aphthosa photosymbiodeme. New Phytologist 139:3 (1998), 517–524.
Philippe, H., Brinkmann, H., Lavrov, D.V., Littlewood, D.T.J., Manuel, M., Wörheide, G., Baurain, D., Resolving difficult phylogenetic questions: why more sequences are not enough. PLoS Biol., 9, 2011, e1000602.
Philippe, H., de Vienne, D.M., Ranwez, V., Roure, B., Baurain, D., Delsuc, F., Pitfalls in supermatrix phylogenomics. Eur. J. Taxon. 283 (2017), 1–25.
Popa, O., Landan, G., Dagan, T., Phylogenomic networks reveal limited phylogenetic range of lateral gene transfer by transduction. ISME J., 11(2), 2017, 543.
Ran, L., Larsson, J., Vigil-Stenman, T., Nylander, J.A.A., Ininbergs, K., Zheng, W.-W., Lapidus, A., Lowry, S., Haselkorn, R., Bergman, B., Genome erosion in a nitrogen-fixing vertically transmitted endosymbiotic multicellular cyanobacterium. PLoS ONE, 5, 2010, e11486.
Robinson, D.F., Foulds, L.R., Comparison of phylogenetic trees. Math. Biosci. 53:1–2 (1981), 131–147.
Rodriguez, F.J.L.O.J., Oliver, J.L., Marin, A., Medina, J.R., The general stochastic model of nucleotide substitution. J. Theor. Biol. 142:4 (1990), 485–501.
Rodríguez, A., Burgon, J.D., Lyra, M., Irisarri, I., Baurain, D., Blaustein, L., Göçmen, B., Künzel, S., Mable, B.K., Nolte, A.W., Veith, M., Inferring the shallow phylogeny of true salamanders (Salamandra) by multiple phylogenomic approaches. Mol. Phylogenet. Evol. 115 (2017), 16–26.
Rolland, T., Neuvéglise, C., Sacerdot, C., Dujon, B., Insertion of horizontally transferred genes within conserved syntenic regions of yeast genomes. PLoS ONE, 4(8), 2009, e6515.
Roure, B., Rodriguez-Ezpeleta, N., Philippe, H., SCaFoS: a tool for selection, concatenation and fusion of sequences for phylogenomics. BMC Evol. Biol., 7, 2007, S2.
Shi, T., Falkowski, P.G., Genome evolution in cyanobacteria: the stable core and the variable shell. PNAS 105 (2008), 2510–2515.
Shih, P.M., Wu, D., Latifi, A., Axen, S.D., Fewer, D.P., Talla, E., Calteau, A., Cai, F., de Marsac, N.T., Rippka, R., Herdman, M., Improving the coverage of the cyanobacterial phylum using diversity-driven genome sequencing. PNAS 110 (2013), 1053–1058.
Simion, P., Philippe, H., Baurain, D., Jager, M., Richter, D.J., Di Franco, A., Roure, B., Satoh, N., Quéinnec, É., Ereskovsky, A., Lapebie, P., A large and consistent phylogenomic dataset supports sponges as the sister group to all other animals. Curr. Biol. 27 (2017), 958–967.
Skaloud, P., Peksa, O., Evolutionary inferences based on ITS rDNA and actin sequences reveal extensive diversity of the common lichen alga Asterochloris (Trebouxiophyceae, Chlorophyta). Mol. Phylogenet. Evol. 54:1 (2010), 36–46.
Snir, S., Rao, S., Quartet MaxCut: a fast algorithm for amalgamating quartet trees. Mol. Phylogenet. Evol. 62:1 (2012), 1–8.
Stamatakis, A., RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22 (2006), 2688–2690.
Stamatakis, A., Hoover, P., Rougemont, J., A rapid bootstrap algorithm for the RAxML web servers. Syst. Biol. 57 (2008), 758–771.
Stöver, B.C., Müller, K.F., TreeGraph 2: combining and visualizing evidence from different phylogenetic analyses. BMC Bioinf., 11(1), 2010, 7.
Stuart, R.K., Mayali, X., Lee, J.Z., Craig Everroad, R., Hwang, M., Bebout, B.M., Weber, P.K., Pett-Ridge, J., Thelen, M.P., Cyanobacterial reuse of extracellular organic carbon in microbial mats. ISME J. 10 (2016), 1240–1251.
Swofford, D.L., 2003. PAUP*: phylogenetic analysis using parsimony, version 4.0 b10.
Taboada, B., Estrada, K., Ciria, R., Merino, E., Operon-mapper: a web server for precise operon identification in bacterial and archaeal genomes. Bioinformatics 34 (2018), 4118–4120.
Tekaia, F., Inferring orthologs: open questions and perspectives. Genomics Insights 9 (2016), 17–28.
Thompson, J.N., The evolution of species interactions. Science 284:5423 (1999), 2116–2118.
Tooming-Klunderud, A., Sogge, H., Rounge, T.B., Nederbragt, A.J., Lagesen, K., Glöckner, G., et al. From green to red: horizontal gene transfer of the phycoerythrin gene cluster between planktothrix strains. Appl. Environ. Microbiol. 79 (2013), 6803–6812.
U'Ren, J.M., Lutzoni, F., Miadlikowska, J., Arnold, A.E., Community analysis reveals close affinities between endophytic and endolichenic fungi in mosses and lichens. Microb. Ecol. 60:2 (2010), 340–353.
Voß, B., Bolhuis, H., Fewer, D.P., Kopf, M., Möke, F., Haas, F., El-Shehawy, R., Hayes, P., Bergman, B., Sivonen, K., Dittmann, E., Insights into the physiology and ecology of the brackish-water-adapted cyanobacterium Nodularia spumigena CCY9414 based on a genome-transcriptome analysis. PLoS ONE, 8(3), 2013, e60224.
Warshan, D., Liaimer, A., Pederson, E., Kim, S.Y., Shapiro, N., Woyke, T., Altermark, B., Pawlowski, K., Weyman, P.D., Dupont, C.L., Rasmussen, U., Genomic changes associated with the evolutionary transitions of Nostoc to a plant symbiont. Mol. Biol. Evol. 35:5 (2018), 1160–1175.
Xi, Z., Rest, J.S., Davis, C.C., Phylogenomics and coalescent analyses resolve extant seed plant relationships. PLoS ONE, 8(11), 2013, e80870.
Zhang, J., Fu, X.X., Li, R.Q., Zhao, X., Liu, Y., Li, M.H., Zwaenepoel, A., Ma, H., Goffinet, B., Guan, Y.L., Xue, J.Y., The hornwort genome and early land plant evolution. Nat. Plants 6:2 (2020), 107–118.
Zhaxybayeva, O., Gogarten, J.P., Charlebois, R.L., Doolittle, W.F., Papke, R.T., Phylogenetic analyses of cyanobacterial genomes: quantification of horizontal gene transfer events. Genome Res. 16 (2006), 1099–1108.
Zolan, M.E., Pukkila, P.J., Inheritance of DNA methylation in Coprinus cinereus. Mol. Cell. Biol. 6:1 (1986), 195–200.