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Origin of Magnetotaxis: Vertical Inheritance Or Horizontal Transfer? Sishuo Wang (王思硕)A,B,1 and Youhua Chen (陈有华)C

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Origin of Magnetotaxis: Vertical Inheritance Or Horizontal Transfer? Sishuo Wang (王思硕)A,B,1 and Youhua Chen (陈有华)C LETTER LETTER Origin of magnetotaxis: Vertical inheritance or horizontal transfer? Sishuo Wang (王思硕)a,b,1 and Youhua Chen (陈有华)c Lin et al. (1) claim that the origin of magnetotaxis dates An alternative explanation is horizontal gene trans- back to the Archean using phylogenomic methods. fer (HGT). The authors exclude the possibility of HGT Although we salute the interesting results, we have based on the consistency between the phylogeny of serious concerns about their fundamental conclusion magnetosome genes and the taxonomic phylogeny and interpretation of the results. and the similar substitution rate per synonymous site The dating of the origin of magnetotaxis was based (dS) between magnetosome genes and three house- on the inference of a magnetotactic ancestor of Proteo- keeping genes (1). However, the power of their de- bacteria and Nitrospirae phyla. However, whether the tection of HGT is largely limited by the small number ancestor of Proteobacteria and Nitrospirae is magneto- of MTB (as shown in figure 1B of ref. 1) (4). Also, dS was tactic is highly questionable. The biggest problem with likely saturated due to the long evolutionary distance their explanation is that it requires the assumption of an between analyzed species, making the comparison of enormous number of independent losses of magneto- dS unconvincing (5). Therefore, it is possible that mag- some genes in all lineages except for the direct ances- netosome genes originated in Alphaproteobacteria tors of magnetotactic species (2). Also, the sampling of and were acquired by some species from Nitrospirae species in their phylogeny is very limited and biased: and Deltaproteobacteria via ancient HGT followed by 30% of the species are outgroup species, and in Pro- limited losses of magnetosome genes within each teobacteria where most magnetotactic bacteria (MTB) lineage (3, 6, 7). If so, the origin of MTB should be were found, only 25 species from five orders were pre- no earlier than the divergence of Alphaproteobacte- sent (as shown in their figure S5) (1). ria, which is around 2.0 giga annum (Ga) (8, 9). Also, To further assess the possibility of a magnetotactic magnetosome genes might be transferred from un- ancestor of Proteobacteria and Nitrospirae, we care- known or extinct lineages to extant MTB (2, 10). In fully selected 258 representative species covering either case, HGT can greatly simplify the evolutionary 32 orders and reconstructed the species phylogeny. scenario of MTB as it not only avoids assuming a be- Assuming that the ancestor of Proteobacteria and wildering number of parallel gene losses but also well Nitrospirae is an MTB, the loss of the entire cluster explains the sporadic distribution of MTB (2). of magnetosome genes has to be assumed to occur In summary, vertical inheritance alone is insufficient at least 26 times (Fig. 1). To the best of our knowledge, to interpret the evolution of MTB given the genomic no precedence of such a large number of gene losses data available. Hence, the origin of magnetotaxis has been described. Thus, our result strongly argues during the Archean, which is based on the inference against the origin of MTB before the divergence of of a magnetotactic ancestor of Proteobacteria and Proteobacteria and Nitrospirae (3). Nitrospirae, is highly speculative. aBeaty Biodiversity Centre, University of British Columbia, Vancouver, BC, Canada, V6T 1Z4; bDepartment of Botany, Faculty of Science, University of British Columbia, Vancouver, BC, Canada, V6T 1Z4; and cDepartment of Renewable Resources, Faculty of Agricultural, Life and Environmental Sciences, University of Alberta, Edmonton, AB, Canada, T6G 2H1 Author contributions: S.W. designed research; S.W. performed research; S.W. and Y.C. analyzed data; and S.W. and Y.C. wrote the paper. The authors declare no conflict of interest. 1To whom correspondence should be addressed. Email: [email protected]. E5016–E5018 | PNAS | June 27, 2017 | vol. 114 | no. 26 www.pnas.org/cgi/doi/10.1073/pnas.1706937114 Downloaded by guest on September 23, 2021 Outgroup Nitrospirae ε Desulfovibrionales δ Syntrophobacterales + Desulfobacterales + Desulfarculales γ Enterobacterales + Vibrionales + Pasteurellales β Rhodospirillales α Sphingomonadales+ Rhodobacterales + Rhizobiales + Caulobacterales Fig. 1. The evolution of MTB in Proteobacteria and Nitrospirae. The phylogeny of Proteobacteria and Nitrospirae was inferred based on 16S rRNA sequence. GTR+G+I was selected as the best-fit substitution model using jModelTest, version 2.1.2, before phylogeny reconstruction. The maximum-likelihood tree of 16S rRNA was constructed using RAxML, version 8.2.4, with 200 times of bootstrap. The number next to the node denotes the bootstrap value. Only bootstrap values ≥ 50 are shown. Lineages of MTB are in blue. Losses of magnetosome genes were inferred, using the parsimonious method assuming the vertical inheritance of magnetosome genes from a magnetotactic ancestor of Proteobacteria and Nitrospirae, and are indicated by a red cross adjacent to the branch. The original tree is available at https://figshare.com/articles/ 16S_rRNA_tree_of_Proteobacteria_and_Nitrospirae/4897181. Wang and Chen PNAS | June 27, 2017 | vol. 114 | no. 26 | E5017 Downloaded by guest on September 23, 2021 1 Lin W, et al. (2017) Origin of microbial biomineralization and magnetotaxis during the Archean. Proc Natl Acad Sci USA 114:2171–2176. 2 Fournier GP, Huang J, Gogarten JP (2009) Horizontal gene transfer from extinct and extant lineages: Biological innovation and the coral of life. Philos Trans R Soc Lond B Biol Sci 364:2229–2239. 3 Kolinko S, Richter M, Glöckner FO, Brachmann A, Schüler D (2016) Single-cell genomics of uncultivated deep-branching magnetotactic bacteria reveals a conserved set of magnetosome genes. Environ Microbiol 18:21–37. 4 Langille MG, Brinkman FS (2009) Bioinformatic detection of horizontally transferred DNA in bacterial genomes. F1000 Biol Rep 1:25. 5 Gojobori T (1983) Codon substitution in evolution and the “saturation” of synonymous changes. Genetics 105:1011–1027. 6 Jogler C, et al. (2011) Conservation of proteobacterial magnetosome genes and structures in an uncultivated member of the deep-branching Nitrospira phylum. Proc Natl Acad Sci USA 108:1134–1139. 7 Lefèvre CT, et al. (2013) Comparative genomic analysis of magnetotactic bacteria from the Deltaproteobacteria provides new insights into magnetite and greigite magnetosome genes required for magnetotaxis. Environ Microbiol 15:2712–2735. 8 Battistuzzi FU, Feijao A, Hedges SB (2004) A genomic timescale of prokaryote evolution: Insights into the origin of methanogenesis, phototrophy, and the colonization of land. BMC Evol Biol 4:44. 9 Sheridan PP, Freeman KH, Brenchley JE (2003) Estimated minimal divergence times of the major bacterial and archaeal phyla. Geomicrobiol J 20:1–14. 10 Ji B, et al. (2017) The chimeric nature of the genomes of marine magnetotactic coccoid-ovoid bacteria defines a novel group of Proteobacteria. Environ Microbiol 19:1103–1119. E5018 | www.pnas.org/cgi/doi/10.1073/pnas.1706937114 Wang and Chen Downloaded by guest on September 23, 2021.
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