Detection of Horizontal Gene Transfer in the Genome of the Choanoflagellate Salpingoeca Rosetta

Overview

Journal Sci Rep

Specialty Science

Date 2021 Mar 17

PMID 33727612

Citations 6

Authors

Danielle M Matriano

Rosanna A Alegado

Cecilia Conaco

Affiliations

Soon will be listed here.

Abstract

Horizontal gene transfer (HGT), the movement of heritable materials between distantly related organisms, is crucial in eukaryotic evolution. However, the scale of HGT in choanoflagellates, the closest unicellular relatives of metazoans, and its possible roles in the evolution of animal multicellularity remains unexplored. We identified at least 175 candidate HGTs in the genome of the colonial choanoflagellate Salpingoeca rosetta using sequence-based tests. The majority of these were orthologous to genes in bacterial and microalgal lineages, yet displayed genomic features consistent with the rest of the S. rosetta genome-evidence of ancient acquisition events. Putative functions include enzymes involved in amino acid and carbohydrate metabolism, cell signaling, and the synthesis of extracellular matrix components. Functions of candidate HGTs may have contributed to the ability of choanoflagellates to assimilate novel metabolites, thereby supporting adaptation, survival in diverse ecological niches, and response to external cues that are possibly critical in the evolution of multicellularity in choanoflagellates.

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References

Eyres I, Boschetti C, Crisp A, Smith T, Fontaneto D, Tunnacliffe A . Horizontal gene transfer in bdelloid rotifers is ancient, ongoing and more frequent in species from desiccating habitats. BMC Biol. 2015; 13:90. PMC: 4632278. DOI: 10.1186/s12915-015-0202-9. View

Southworth J, Armitage P, Fallon B, Dawson H, Bryk J, Carr M . Patterns of Ancestral Animal Codon Usage Bias Revealed through Holozoan Protists. Mol Biol Evol. 2018; 35(10):2499-2511. PMC: 6188563. DOI: 10.1093/molbev/msy157. View

Huang J . Horizontal gene transfer in eukaryotes: the weak-link model. Bioessays. 2013; 35(10):868-75. PMC: 4033532. DOI: 10.1002/bies.201300007. View

Wellner A, Lurie M, Gophna U . Complexity, connectivity, and duplicability as barriers to lateral gene transfer. Genome Biol. 2007; 8(8):R156. PMC: 2374987. DOI: 10.1186/gb-2007-8-8-r156. View

Tucker R, Beckmann J, Leachman N, Scholer J, Chiquet-Ehrismann R . Phylogenetic analysis of the teneurins: conserved features and premetazoan ancestry. Mol Biol Evol. 2011; 29(3):1019-29. PMC: 3278476. DOI: 10.1093/molbev/msr271. View

Llosa M, Gomis-Ruth F, Coll M, de la Cruz Fd F . Bacterial conjugation: a two-step mechanism for DNA transport. Mol Microbiol. 2002; 45(1):1-8. DOI: 10.1046/j.1365-2958.2002.03014.x. View

Fan X, Qiu H, Han W, Wang Y, Xu D, Zhang X . Phytoplankton pangenome reveals extensive prokaryotic horizontal gene transfer of diverse functions. Sci Adv. 2020; 6(18):eaba0111. PMC: 7190310. DOI: 10.1126/sciadv.aba0111. View

Kumar S, Stecher G, Li M, Knyaz C, Tamura K . MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms. Mol Biol Evol. 2018; 35(6):1547-1549. PMC: 5967553. DOI: 10.1093/molbev/msy096. View

Castresana J . Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol. 2000; 17(4):540-52. DOI: 10.1093/oxfordjournals.molbev.a026334. View

10.

Soucy S, Huang J, Gogarten J . Horizontal gene transfer: building the web of life. Nat Rev Genet. 2015; 16(8):472-82. DOI: 10.1038/nrg3962. View

11.

Southworth J, Grace C, Marron A, Fatima N, Carr M . A genomic survey of transposable elements in the choanoflagellate reveals selection on codon usage. Mob DNA. 2019; 10:44. PMC: 6875170. DOI: 10.1186/s13100-019-0189-9. View

12.

Hildebrand F, Meyer A, Eyre-Walker A . Evidence of selection upon genomic GC-content in bacteria. PLoS Genet. 2010; 6(9):e1001107. PMC: 2936529. DOI: 10.1371/journal.pgen.1001107. View

13.

Woznica A, Cantley A, Beemelmanns C, Freinkman E, Clardy J, King N . Bacterial lipids activate, synergize, and inhibit a developmental switch in choanoflagellates. Proc Natl Acad Sci U S A. 2016; 113(28):7894-9. PMC: 4948368. DOI: 10.1073/pnas.1605015113. View

14.

Jeuck A, Arndt H, Nitsche F . Extended phylogeny of the Craspedida (Choanomonada). Eur J Protistol. 2014; 50(4):430-43. DOI: 10.1016/j.ejop.2014.06.001. View

15.

Daubin V, Lerat E, Perriere G . The source of laterally transferred genes in bacterial genomes. Genome Biol. 2003; 4(9):R57. PMC: 193657. DOI: 10.1186/gb-2003-4-9-r57. View

16.

Ruiz-Trillo I, Roger A, Burger G, Gray M, Lang B . A phylogenomic investigation into the origin of metazoa. Mol Biol Evol. 2008; 25(4):664-72. DOI: 10.1093/molbev/msn006. View

17.

Mizrokhi L, Mazo A . Evidence for horizontal transmission of the mobile element jockey between distant Drosophila species. Proc Natl Acad Sci U S A. 1990; 87(23):9216-20. PMC: 55135. DOI: 10.1073/pnas.87.23.9216. View

18.

Doolittle W . You are what you eat: a gene transfer ratchet could account for bacterial genes in eukaryotic nuclear genomes. Trends Genet. 1998; 14(8):307-11. DOI: 10.1016/s0168-9525(98)01494-2. View

19.

Chen I, Dubnau D . DNA uptake during bacterial transformation. Nat Rev Microbiol. 2004; 2(3):241-9. DOI: 10.1038/nrmicro844. View

20.

Lercher M, Pal C . Integration of horizontally transferred genes into regulatory interaction networks takes many million years. Mol Biol Evol. 2007; 25(3):559-67. DOI: 10.1093/molbev/msm283. View