Rampant HGT in microbial Rampant HGT in microbial eukaryotes

Rampant HGT in microbialeukaryotesCheong Xin Chan (C.X.)cx-chan@uiowa.eduDepartment t of Biology &Roy J. Carver Center for Comparative GenomicsThe University of IowaDepartment of Ecology, Evolution & Natural Resources &Institute t of Marine and Coastal SciencesRutgers University as of July 1, 2009SMBE 2009, Iowa City, IA. 4 June 2009

IntroductionHorizontal gene transfer (HGT)Doolittle WF(1999). Science284: 2124-2128.Transfer of genetic materials between non-lineal organisms2

1992 PNAS, 89: 8990-42005 PNAS, 102: 14332-72007 Science, 317: 1753-62008PNAS, 105: 17867-712009MBE, 26: 367-743

IntroductionEndosymbiosis Endosymbiotic gene & evolution transfer of (EGT)eukaryotesSecondary EGTPrimaryEGT4

ObjectivesHGT in microbial eukaryotes• To examine the gene origins, i.e., extent ofHGT/EGT in microbial eukaryotes• To examine the potential impact of HGT/EGTin these organisms on the reconstruction ofthe eukaryote tree of life5

EGT & HGT in Dinoflagellates- Involvement of tertiary endosymbiosis(Yoon et al., 2005, MBE; Nosenko et al., 2006, MBE)- Tertiary EGT(e.g., eukaryote-eukaryote gene transfer)- EGT & HGT: key contributors to the genomemake-up- Genes are expected to have a variety ofevolutionary histories (to have come fromvarious sources of other lineages)- Genomes are expected to be highly chimeric7

DinoflagellatesAlexandrium tamarensehttp://www.whoi.edu/science/B/redtide/species/alexandrium_images.htmlhttp://www.whoi.edu/redtide/page.do?pid=24595http://serc.carleton.edu/images/microbelife/topics/red_tide_for_ed.jpghttp://www.whoi.edu/cms/images/5_47876.jpg- Heterotrophic primary marineproducers, peridinin-containing- Each cell is ~25-46 µm in length- Causative agent of “red tide” (HAB)- Produces saxitoxin (a neurotoxin)- Causes paralytic shellfish h poisoningi(PSP)- Limited genomic data 8

MethodologyGenome make-up of dinoflagellatesAlexandrium tamarense ESTs(12,329)Phylogenomic pipelineML & BayesianMoustafa*, Chan* et al., (2008). Genome Informatics 21: 165-176.9

Results & DiscussionGenome make-up of dinoflagellates• One-half of the genes in A. tamarense encode novelfunctions• A. tamarense genes have diverse taxonomic origins• Chromalveolates and Plantae are major partners ofgene sharing in dinoflagellates• Most genes from Plantae are from the green algae• Novel observation of GT instances (440) between thehaptophytes (Emiliania huxleyi) to peridinindinoflagellates• Transferred genes with variety of functions, proteintargets not limited to chloroplast and mitochondria11

Results & DiscussionGreen genes in dinoflagellateshttp://www.morning-earth.org/Micromonas pusilahttp://genome.jgi-psf.org/Ost9901_3/Ostta.jpgPrasinophytes- Anciently derived green algae,picoeukaryotes- Each cell is < 2 µm in length- Likely candidates for crypticendosymbionts- Genomes of Micromonas andOstreococcus have recentlybeen completely sequenced,providing a sizeable gene poolfor analysisOstreococcus12

fucoxanthin dinoperidinin dinoTertiaryendosymbiosis• 125 prasinophyte-derived gene indinoflagellates• Possible explanations:• (a) HGT from a prasinophyte source, or• (b) massive gene loss in all other chromalveolatelineages• Example also shows putative EGT betweenhaptophyte lineage with the fucoxanthindinoflagellates(as expected in tertiary endosymbiosis)13

Results & DiscussionHaptophyte-derived genes in dinoflagellates• 400+ haptophyte-derived genes in A.tamarense (a peridinin dinoflagellate)• 382 from Emiliania huxleyi (of which completegenome is available)• These genes encode various transferases andother proteins crucial to cellular processes15

peridinin dinofucoxanthin dinoSPDS gene family (spermidine synthase)16

Results & DiscussionHaptophyte-derived genes in dinoflagellatesWhat does that tell us?• Another “hidden” endosymbiosisin chromalveolates l at the baseof dinoflagellates – these genesare instances of EGT• Haptophytes are common preyfor early diverging peridinindinoflagellates – these genesare instances of HGT17

Results & DiscussionEffects on inferring the tree of life• At least 32.4% of the total ESTs in this study showHGT history• The number represents a conservative estimate• Limited by HGT detectibility and taxon sampling• 387 (3.1%) “informational/structural” genes show noevidence of HGT – represent signals of verticalinheritance• Chimeric i genomes of microbial eukaryotescomplicate the resolution of these lineages on thetree of life18

Conclusions• HGT among microbial eukaryotes is comparable to thosereported in prokaryotes• Phylogenetic markers that are useful for delineatingrelationships within other groups might proved inappropriatewhen applied to dinoflagellates (and chromalveolates)• Higher cellular complexity & greater gene coding capacity inmicrobial eukaryotes (compared to prokaryotes) do notconstitute significant barriers to HGT• HGT in microbial eukaryotes are rampant• Many of these organisms are found in harsh and highlyvariable aquatic environments – they acquire foreign genes torepair, replace or provide novel traits to adapt to changingenvironmental conditions19

AcknowledgementsBhattacharya GroupDebashish BhattacharyaAhmed MoustafaAdrián Reyes-PrietoValérie ReebBill LanierHeather TyraJeferson GrossNIH grant R01ES013679SMBE 2009, Iowa City, IA. 4 June 200920. The End