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Horizontal Gene Transfer in Choanoflagellates

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Horizontal Gene Transfer in Choanoflagellates REVIEW Horizontal Gene Transfer in Choanoflagellates RICHARD P. TUCKER* Department of Cell Biology and Human Anatomy, University of California, Davis, Davis, California ABSTRACT Horizontal gene transfer (HGT), also known as lateral gene transfer, results in the rapid acquisition of genes from another organism. HGT has long been known to be a driving force in speciation in prokaryotes, and there is evidence for HGT from symbiotic and infectious bacteria to metazoans, as well as from protists to bacteria. Recently, it has become clear that as many as a 1,000 genes in the genome of the choanoflagellate Monosiga brevicollis may have been acquired by HGT. Interestingly, these genes reportedly come from algae, bacteria, and other choanoflagellate prey. Some of these genes appear to have allowed an ancestral choanoflagellate to exploit nutrient-poor environments and were not passed on to metazoan descendents. However, some of these genes are also found in animal genomes, suggesting that HGT into a common ancestor of choanozoans and animals may have contributed to metazoan evolution. J. Exp. Zool. (Mol. Dev. Evol.) 320B:1–9, 2013. © 2012 Wiley Periodicals, Inc. J. Exp. Zool. (Mol. Dev. Evol.) How to cite this article: Tucker RP. 2013. Horizontal gene transfer in choanoflagellates. J. Exp. 320B:1–9, 2013 Zool. (Mol. Dev. Evol.) 320B:1–9. A key event that can contribute to the evolution of a species is the these are intracellular pathogens that have been infecting protists acquisition of new genetic material. This can take a number of for a very long time. Nevertheless, it points to the potential for the different forms ranging from point mutations to chromosomal two-way acquisition of potentially beneficial genes across recombination and rearrangements to whole genome duplica- kingdoms. tions; the inheritance of, and selection for, the novel genetic Choanoflagellates are now widely considered to be the most material derived from pre-existing genes can lead to distinctive closely related group to metazoans (Fig. 1A; King and Carroll, traits that are the hallmark of a novel species. In prokaryotes it has 2001; Philippe et al., 2004; Abedin and King, 2008; King et al., been recognized for decades that new genetic material in the form 2008, 2009). Intriguingly, examination of choanoflagellate genes of complete, novel genes can be acquired through horizontal indicates that HGT is particularly common in these single-celled gene transfer (HGT; also referred to a lateral gene transfer; organisms, with genes appearing to arise from prokaryotic and Lawrence, '99; de la Cruz and Davies, 2000). This can be a eukaryotic prey caught in the mucous net arrayed between relatively common event. Early studies predicted that between 8% microvilli at the base of their flagellum (Fig. 1B–D). Here, I will and 18% of the Escherichia coli genome was acquired by HGT review the recent (and rapidly growing) literature supporting HGT (Ochman and Lawrence, '96), and more recent studies comparing in the choanoflagellate genus Monosiga and present novel the genomes of different E. coli strains suggest that HGT may even analyses of these genes taking into consideration the number of be more common (e.g., Brzuszkiewicz et al., 2006; reviewed by novel genomes that have become available since the original Dobrindt et al., 2010). research was done. HGT is not limited to prokaryotes. Recently, HGT from bacteria to arthropods and nematodes, as well as from bacteria to hydrozoans, has been described (Dunning Hotopp, 2011). For example, approximately 30% of the genome of the proteobacteria Conflict of interest: none to declare. Wolbachia, a parasitic microbe of arthropods, is found in the *Correspondence to: Richard P. Tucker, Department of Cell Biology and genome of the beetle Callosobruchus chinensis (Nikoh et al., 2008). Human Anatomy, University of California, Davis, Davis, CA 95616. E-mail: [email protected] There is even evidence of HGT from eukaryotes to bacteria: Received 20 December 2011; Revised 25 May 2012; Accepted 20 August approximately 100 genes in Legionella pneumophila, the bacteria 2012 behind Legionnaire's Disease, appear to have a protist origin Published online 19 September 2012 in Wiley Online Library (wiley (Lurie-Weinberger et al., 2010). The number of eukaryote-derived onlinelibrary.com). genes in L. pneumophila is likely to be unusually high given that DOI: 10.1002/jez.b.22480 © 2012 WILEY PERIODICALS, INC. 2 TUCKER Figure 1. A schematic tree of life showing plausible phylogenetic relationships between choanoflagellates, fungi, and metazoans (A). Choanoflagellates are characterized by a microvilli collar found at the apical end of the cell body (B). A flagellum creates currents that can drive algal and prokaryotic prey into a mucous net arrayed between the microvilli (C). The prey are then phagocytosed, creating the potential for horizontal gene transfer (D). PHOSPHOFRUCTOKINASE: THE FIRST EXAMPLE OF most similar to PFK sequences encoded in prokaryotic genomes HORIZONTAL GENE TRANSFER INTO CHOANOZOANS (e.g., it shares 62% amino acid identity with PFK from the The first description of HGT between a prokaryote and a photosynthetic acidobacteria Chloracidobacterium thermophi- choanoflagellate is found in Bapteste et al. (2003). This article lum, AEP13132), and among eukaryotic sequences it is most describes the complex evolutionary history of phosphofructoki- similar to PFK from plants (e.g., 45% amino acid identity with nase (PFK), a highly conserved enzyme that is central to the PFK from Arabidopsis thaliana, AAL90928). Interestingly, the canonical glycolytic pathway. Construction of a phylogenetic tree PFK from M. brevicollis (XP_001742461) is more similar to the based on the PFK sequences from a number of species resulted in PFKs found in fungi and metazoa that the PFK from M. ovata. puzzling relationships, not the least of which was the grouping of When these and other representative sequences are aligned with a PFK from Monosiga ovata with PFKs from the spirochetes ClustalW (http://www.genome.jp/tools/clustalw/) (Pairwise Borrelia brugdorferi and Treponema sp. Such groupings are alignment parameters = gap open penalty:10.0; gap extension typically considered to be evidence of HGT. The authors concluded penalty:0.01; Mulitple alignment parameters = gap open penal- that this unusual relationship argued for HGT between the gram ty:10.0; gap extension penalty:0.05; no weight transition; negative bacteria and the choanoflagellate, and that this was one hydrophobic residues:GPSNDQERK) and the sequences aligning of many cases where PFK and genes encoding related enzymes with the first 243 amino acids of the M. ovata enzyme (which may have passed from one genome to another by HGT. Evidence align with few gaps) are subjected to simple phylogenetic tree for the expression of this PFK in M. ovata is supported by the analysis(UPGMA;fromthe ClustalWsite),itisclearthat thegene presence of ESTs (Table 1). in M. ovata that came from a prokaryote via HGT does not sort Reanalysis of the possible origins of PFK were undertaken by with the homolog from M. brevicollis, and that a gene related to using the default parameters of tblastn (http://blast.ncbi.nlm. the one in M. brevicollis, and not the gene that arose by HGT, was nih.gov/) and searching the NCBI nucleotide collection. As likely to be the gene that ultimately was contributed to the reported by Bapteste et al. (2003), the M. ovata PFK sequence is metazoan genome (Table 2; Fig. 2A). J. Exp. Zool. (Mol. Dev. Evol.) HORIZONTAL GENE IN CHOANOFLAGELLATES 3 Table 1. Representative genes reported to be acquired by choanoflagellates via horizontal gene transfer. Protein name RefSeq/JGI ID Putative origin EST?a Refs. Phosphofructokinase AAQ55175b Bacteria Yes Bapteste et al. (2003) Spo11-3 EDQ87716 Algae No Malik et al. (2007) Top6B XP_001744261 Algae No Malik et al. (2007) Uroporphyrin III methyltransferase XP_001742170 Cyanobacteria No Maruyama et al. (2009) Cobalamin synthesis protein XP_001746731 Cyanobacteria No Maruyama et al. (2009) Amino acid aminotransferase XP_001749475 Cyanobacteria Yes Maruyama et al. (2009) Glyoxalase I family-like protein XP_001750995 Cyanobacteria No Maruyama et al. (2009) lysA XP_001746610 Bacteria Yes Torruella et al. (2009) Ammonium transporter 1 XP_001743145 Algae No Nedelcu et al. (2009) Glutamine synthetase 32625 Algae Yes Nedelcu et al. (2009) Glutamate synthase 15256 Algae No Nedelcu et al. (2009) thrA 34304 Algae Yes Sun and Huang (2011) ilvD 32689 Algae Yes Sun and Huang (2011) ilvE 32828 Diatom Yes Sun and Huang (2011) Teneurin XP_001749414 Diatom/bacteria Yes Tucker et al. (2012) aAs determined from reference or by tblastn of Monosiga sequence against non-human, non-mouse ESTs limited to Monosiga. bMonosiga ovata (RefSeq/JGI ID numbers not indicated by a superscript b are from Monosiga brevicollis). Table 2. Analysis of genes reported to be acquired by choanoflagellates via horizontal gene transfer (HGT). Likely origin HGT gene Pre-existing From Replaces Found with Into homolog into Protein name HGT Prokaryotic Plant homolog homolog Novela metazoa metazoa Phosphofructokinaseb Yes Yes Yesf Yes Spo11-3 Yes Yes Yes Yes Top6B Yes Yes Yes Uroporphyrin III methyltransferase Yes ?c ?e Yes Cobalamin synthesis proteinb Yes Yes Yes Amino acid aminotransferase Yes Yes ? Glyoxalase I family-like protein Yes ?e lysA Yes Yes ? ? ? Ammonium transporter 1 Yes Yes Yes Yes Glutamine synthetaseb Yes Yes Yes Yes Glutamate synthase Yes Yes Yes Yes thrA Yes ? ? Yes ilvD Yes Yes Yes Yes Yes Yes ilvE Yes Yes ? Teneurinb Yes Yesd Yes Yes aHomologous gene not found in amoebozoa or fungi, suggesting that gene appeared in unikonts via HGT. bPhylogenetic trees are provided elsewhere. cAnalysis inconclusive. dA fusion of domains acquired by HGT and a pre-existing transmembrane protein. ePossible origin from an oomycete. fReplaces homolog in Monosiga ovata, but pre-existing gene is found in M. brevicollis. J. Exp. Zool. (Mol. Dev. Evol.) 4 TUCKER Figure 2. Phylogenetic tree analysis of representative proteins proposed to have been acquired in choanozoans by horizontal gene transfer (see text for details).
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