Examples of inter-phylum adaptive horizontal DNA transfers based on genomic data

Donor

Recipient

Function(s)

Reference(s)

Prokaryote-prokaryote (Koonin 2016)

Bacteria

Methanogenic Archaea

(early Haloarchaea)

1,089 transfers, carbon metabolism, membrane transporters, menaquinone biosynthesis, and complexes I-IV of the eubacterial respiratory chain; converted strictly anaerobic, chemolithoautotrophic methanogen into heterotrophic, oxygen-respiring haloarchaeal common ancestor.

(Nelson-Sathi, Dagan et al. 2012)

Bacteria

Methanogenic Archaea Methosarcina spp.

~5-11% of genetic loci, including gluconeogenesis, proline biosynthesis, transport processes, DNA-repair, environmental sensing, gene regulation, and stress response, such as the bacterial GroEL/GroES chaperone system and the presence of tetrahydrofolate-dependent enzymes

(Deppenmeier, Johann et al. 2002; Garushyants, Kazanov et al. 2015)

Bacteria

Mesophilic clades descended from thermophilic Archaea: Thaumarchaeota, MG II/III euryarchaeotes, Halobacteriales

Mesophilic metabolic activites (energy conversion, amino acid transport and metabolism, and lipid or membrane biogenesis): Thaumarchaeota (937 loci), MG II/III euryarchaeotes (1677 loci), Halobacteriales (1047 loci)

(Deschamps, Zivanovic et al. 2014; Lopez-Garcia, Zivanovic et al. 2015)

Bacteria

Early Archaeal progenitors

“13 archaeal higher taxa…correspond to 2,264 group-specific gene acquisitions from bacteria”

(Nelson-Sathi, Sousa et al. 2015; Groussin, Boussau et al. 2016)

Prokaryote-eukaryote microbe (Marcet-Houben and Gabaldon 2009; Soanes and Richards 2014)

Actinobacterium

Basidiomycete Agaricomycotina

Alpha-amylase

(Da Lage, Binder et al. 2013)

Bacteria

Plant pathogenic fungi Pyrenophora teres and Pyrenophora tritici-repentis

Extracellular proteins, interference with plant defense-response, degradation of plant cell walls, carbohydrate metabolism

(Sun, Xiao et al. 2013; Soanes and Richards 2014)

Bacteria (40%), fungi (25%), and viruses (22%)

Animal pathogenic fungus Aspergillus fumigatus

Central and intermediary metabolism, virulence (including lipase, 4 peptide transporters, gliotoxin synthesis)

(Mallet, Becq et al. 2010)

Bacteria and Archaea

Red alga Galdieria sulphuraria

Growth in high temperature, toxic metal-rich, acidic environments

(Schonknecht, Chen et al. 2013)

Bacteria

Red alga Porphyridium purpureum

Non-plastid functions encoded in nuclear genome

(Qiu, Yoon et al. 2013)

Actinobacteria, proteobacteria, archaea

Chromalveolates (dinoflagellates of the genera Karenia and Karlodinium)

Energy metabolism, sugar and amino acid metabolism, cell membrane biosynthesis, substrate transport, DNA repair

(Nosenko and Bhattacharya 2007)

Proteobacteria, cyanobacteria and archaea

Diatom Phaeodactylum tricornutum

7.5% of genetic loci (784 loci); organic carbon and nitrogen utilization (xylanases and glucanases, prismane, carbon-nitrogen hydrolase, amidohydrolase), diatom urea cycle (carbamoyl transferase, carbamate kinase, ornithine cyclodeaminase) and polyamine metabolism related to diatom cell wall silicification (S-adenosylmethionine (SAM)-dependent decarboxylases and methyltransferases); also cell wall component synthesis, unorthodox DNA replication, repair and recombination mechanisms

(Bowler, Allen et al. 2008)

Bacteria, archaea

Rumen ciliates

Catabolism of complex carbohydrates

(Ricard, McEwan et al. 2006)

Actinobacteria

Plant pathogenic fungal Phytophthora species

Cutinase

(Belbahri, Calmin et al. 2008)

Bacteria

Fish ciliate scuticociliatosis pathogen Pseudocohnilembus persalinus

Cell adhesion, hemolysis and heme utilization

(Xiong, Wang et al. 2015)

Bacteria, eukaryotes Dictyostelium

discoideum,

Entamoeba histolytica,

Gibberella zeae,

Mastigamoeba balamuthi

 

Diplomonad fish parasite Spironucleus salmonicida

Amino acid metabolism, DNA repair, protein folding, membrane transport, glycolysis/gluconeogenesis, glyoxylate and dicarboxylate metabolism, pentose phosphate pathway, pyruvate metabolism, starch and sucrose metabolism, nitrogen metabolism, oxidative phosphorylation, purine and pyrimidine metabolism

 

(Andersson, Sjogren et al. 2007)

β,γ-Proteobacteria, Chlamydiae, other bacteria

Red alga Cyanidioschyzon

Amino acid, vitamin, lipid, porphyrin biosynthesis; ATP/ADP transport; RNA processing, translation

(Huang and Gogarten 2008)

Arthrobacter

Ascomycete fungi Penicillium canescens and Scopulariopsis sp

Beta-glucuronidase (enables utilization of glucuronides in vertebrate urine)

(Wenzl, Wong et al. 2005)

Rumen bacteria Fibrobacter succinogenes

Rumen fungus Orpinomyces joyonii

Endoglucanase (polysaccharide digestion)

(Garcia-Vallve, Romeu et al. 2000)

Bacteria

Eukaryotic unicellular parasites (Entamoeba histolytica, E. dispar, Trichomonas vaginalis, Giardia lamblia, Trypanosoma brucei, T. cruzi, Plasmodium falciparum)

Amino acid, sugar, nucleotide, lipid, and, energy metabolism, host glycan degradation, vitamin and membrane biosynthesis, translation

(Loftus, Anderson et al. 2005; Alsmark, Sicheritz-Ponten et al. 2009; Alsmark, Foster et al. 2013; Strese, Backlund et al. 2014; Hirt, Alsmark et al. 2015)

Eukaryote microbe–eukaryote microbe (Andersson 2009; Andersson 2009; Soanes and Richards 2014)

Phytopathogenic fungi in genera Magnaporthiopsis  or Colletotrichum

Phytopathogenic fungi in genera Magnaporthiopsis  or Colletotrichum

33-90 horizontally transferred loci enriched for plant cell wall degrading enzymes

(Qiu, Cai et al. 2016)

Fungi

Plant parasitic oomycetes, e.g., Phytophthora ramorum

Secreted proteins for plant cell wall digestion, resisting plant defenses, effector functions

(Richards, Soanes et al. 2011)

Filamentous plant pathogenic Ascomycete fungus Magnaporthe grisea

Filamentous plant Oomycete pathogen Phytophthora sp.

Sugar-transporter, purine permease, extracellular dioxygenase/Protocatechuate 3,4-dioxygenase β-subunit, aldose 1-epimerase (osmotropic lifestyle)

(Richards, Dacks et al. 2006)

Fungal pathogen Stagonospora nodorum

Fungal pathogen Pyrenophora tritici-repentis

ToxA virulence factor, extends host range

(Mehrabi, Bahkali et al. 2011)

Algae, bacteria

Choanoflagellate Monosiga brevicollis

405 genetic loci (4.4% nuclear genome); carbohydrate and amino acid metabolism, 45 transporters, responses to oxidative, osmotic, antibiotic, or heavy metal stresses, biosynthesis of vitamins C and K12, porphyrins and phospholipids.

(Nedelcu, Miles et al. 2008) (Yue, Sun et al. 2013) (Tucker 2013) (Sun, Yang et al. 2010)

Prokaryote-animal (Dunning Hotopp 2011; Alegado and King 2014; Boto 2014)

Bacteria, likely including some related to marine species Vibrio campbellii, Desulfovibrio hydrothermalis, and Arcobacter nitrofigilis

Sponge Amphimedon queenslandica, a model metazoan ancestor (Srivastava, Simakov et al. 2010)

227 loci transferred, including metallopeptidase, carbohydrate metabolism, polymer degradation, transport, proteolysis, nitrogen metabolism, extracellular matrix biosynthesis

(Conaco, Tsoulfas et al. 2016)

Mainly bacteria, but also fungi, protists, and algae

Bdelloid rotifers

8-9% of genetic loci, including toxin degradation, biosynthesis of antioxidants and key metabolites, amino acid metabolism, non-ribosomal peptide synthetases

(Gladyshev, Meselson et al. 2008; Boschetti, Carr et al. 2012; Eyres, Boschetti et al. 2015)

Bacteria, fungi

Bdelloid rotifer, Adineta ricciae

16 cellulolytic enzymes

(Szydlowski, Boschetti et al. 2015)

Bacteria

Sponge Astrosclera willeyana

Biomineralization

(Jackson, Macis et al. 2011)

Bacteria

Starlet sea anemone, Nematostella vectensis

Shikimic acid biosynthesis, glyoxylate cycle

(Kondrashov, Koonin et al. 2006; Starcevic, Akthar et al. 2008)

Bacteria

Cnidarian Hydra magnipapillata

Carbohydrate, lipid, nucleotide, amino acid, cofactor, vitamin and xenobiotic metabolism, glycan biosynthesis; transamination, methylation, and acetylation of sugars, polysaccharides, or glycoproteins; bacterial lipopolysaccharide (LPS) biosynthetic pathway

(Chapman, Kirkness et al. 2010)

Bacteria

Filarial nematode parasite Onchocerca flexuosa

Independence from Wolbachia endosymbionts; synthesis of riboflavin, heme and nucleotides; inosine monophosphate and uridine monophosphate biosynthesis

(McNulty, Foster et al. 2010; McNulty, Abubucker et al. 2012)

Bacteria, chiefly rhizobacteria, and fungi

Plant parasitic nematodes

Cellulose and phytopolymer digestion (multiple transfers to distinct nematode lineages), B vitamin biosynthesis, plant resistance-breaking effector proteins

(Bird, Opperman et al. 2003; Craig, Bekal et al. 2008; Opperman, Bird et al. 2008; Craig, Bekal et al. 2009; Mitreva, Smant et al. 2009; Danchin 2011; Haegeman, Jones et al. 2011; Mayer, Schuster et al. 2011; Scholl and Bird 2011; Paganini, Campan-Fournier et al. 2012; Eves-van den Akker, Laetsch et al. 2016)

Bacteria

Stick and Leaf Insects

Pectinases

(Shelomi, Danchin et al. 2016)

Bacteria

Phytophagous mites and Lepidoptera

Detoxification of plant defense cyanogenic glucosides

(Wybouw, Dermauw et al. 2014)

Bacteria and fungi

Asian longhorned beetle Anoplophora glabripennis

Enzymes involved in digestion of woody plant tissues and detoxification of plant allelochemicals

(McKenna, Scully et al. 2016)

Bacteria and fungi

Herbivorous arthropods (>20 distinct insect and chelicerate species)

Overcoming plant defenses, assimilation of intracellular plant metabolites, digestion of plant cell walls

(Wybouw, Pauchet et al. 2016)

Bacteria

Coffee berry borer beetle, Hypothenemus hampe

Glycosyl hydrolase (galactomannan, major coffee storage polymer, is the substrate)

(Acuna, Padilla et al. 2012)

Bacteria

Silkworm Bombyx mori and related Lepidoptera

Glycosyl hydrolase family, oxidoreductase family, and amino acid metabolism

(Li, Shen et al. 2011)

Archaea, Bacteria, Fungi, Protists, and Plants

26 animal species (4 Caenorhabditis, 12 Drosophila, and 10 primates)

Multiple metabolic functions (biosynthetic and degradative), innate immunity responses, antioxidant activities

(Crisp, Boschetti et al. 2015)

Bacteria

Arthropods, echinoderms, and vertebrates, including platypus and opossum, but not in splacental mammals

Glyoxylate cycle

(Kondrashov, Koonin et al. 2006)

Bacteria, Archaea, fungi and plants

Tardigrade Hypsibius dujardini (desiccation-resistant animals subject to oxidative stress)

17.5% of tardigrade genetic loci, particularly oxidative stress tolerance functions: catalases; DNA repair functions, including recombination proteins and translesion polymerases; polyamine biosynthesis; heat shock chaperones

(Boothby, Tenlen et al. 2015)

Bacteria

Urochordate Ciona intestinalis

Cellulose synthase

(Nakashima, Yamada et al. 2004)

Eukaryotic microbe-animal (Boto 2014)

Fungi

Pea aphid, two-spotted spider mite Tetranychus urticae

Carotenoid pigment biosynthesis, cyanate metabolism

(Moran and Jarvik 2010; Altincicek, Kovacs et al. 2012; Wybouw, Balabanidou et al. 2012)

Algae and other photosynthetic eukaryotes

Tunicate Ciona intestinalis

Molecule transport, cellular regulation and methylation signaling

(Ni, Yue et al. 2012)

Animal-eukaryotic microbe

Arthropod

Microsporidia intracellular parasites Encephalitozoon intestinalis and Encephalitozoon cuniculi

Purine nucleotide phosphorylase, folylpolyglutamate synthase

(Selman, Pombert et al. 2011; Pombert, Selman et al. 2012)

Prokaryote-plant (non-plastid)

Bacteria, Archaea, viruses, and sea anemones

Moss Physcomitrella patens (primitive land plant)

Xylem formation, plant defense, nitrogen recycling, plus biosynthesis of starch, polyamines, hormones and glutathione; actinoporin water stress adaptation

(Hoang, Cho et al. 2009; Yue, Hu et al. 2012)

Bacteria, fungi

Plants

Shikimate biosynthesis, phenylpropanoid pathway leading to synthesis of flavonoids and lignin, TAL transaldolase involved in vascular biogenesis

(Emiliani, Fondi et al. 2009; Yang, Zhou et al. 2015)

Eukarote microbe-plant

Fungi

Plants (Bryophyte Physcomitrella patens and Lycophyte Selaginella moellendorffil)

L-fucose permease sugar transporter, , membrane transporter, bifunctional iucA/iucC siderophore biosynthesis protein, phospholipase/carboxylesterase family protein. Both cases that involve HGT from a fungus to the bryophyte moss P. patens, the HGT is positioned next to a putative transposable element.

(Richards, Soanes et al. 2009)

Plant-microbe

Plants

Bacteria, fungi, amoebozoa

Expansins (plant cell-wall loosening proteins)

(Nikolaidis, Doran et al. 2014)

Plants

Fungi (Basidiomycete Laccaria bicolor, Chytrydiomycete Bhatrachochytrium dendrobatidis, Ascomycete Sclerotinia sclerotiorum)

Phosphate-responsive protein, zinc binding alcohol dehydrogenase, DUF239 domain protein, zinc finger (C2H2 type) protein

(Richards, Soanes et al. 2009)

Plant-plant (Bock 2009; Gao, Ren et al. 2014)

Parasitic plant (Cuscuta sp.)

Host plant (Plantago sp.)

Mitochondrial loci atp1, atp6 and matR

(Mower, Stefanovic et al. 2004; Mower, Stefanovic et al. 2010)

Tetrastigma rafflesiae Miq (obligate host)

Parasitic flowering plant Rafflesia cantleyi Solms-Laubach

Respiration, carbohydrate metabolism, mitochondrial translation, and protein turnover; mitochondrial sequences

(Davis and Wurdack 2004; Xi, Bradley et al. 2012) (Xi, Wang et al. 2013)

Grasses, Panicoideae genera

16 diploid barley (Hordeum) species

Ribosomal RNA (rDNA) sequences

(Mahelka, Krak et al. 2017)

Bryophyte hornworts

Fern

Novel chimeric photoreceptor--neochrome

(Li, Villarreal et al. 2014)

Andropogoneae, Cenchrinae (2 species), and Melinidinae C4 plants

Grass lineage Alloteropsis (4 independent transfers)

C4 photosynthesis activities (phosphoenolpyruvate carboxylase, phosphoenolpyruvate carboxykinase)

(Christin, Edwards et al. 2012)

Plant

Plants (Amborella and others)

Mitochondrial genomes

(Bergthorsson, Adams et al. 2003; Bergthorsson, Richardson et al. 2004; Rice, Alverson et al. 2013; Gandini and Sanchez-Puerta 2017)

Papilionoid legume

Phelipanche aegyptiaca, parasitic species of family Orobanchaceae

albumin 1 KNOTTIN-like proteins

(Zhang, Fernandez-Aparicio et al. 2013)

Brassicaceae host plant

Root parasitic plant Orobanche aegyptiaca, shoot parasitic plant Cuscuta australis

Strictosidine synthase (independent transfers)

(Zhang, Qi et al. 2014)

Animal-animal

(Boto 2014)

 

 

Fish (herring or sea raven)

Rainbow smelt, Osmerus mordax

Type II anti-freeze protein

(Graham, Lougheed et al. 2008; Graham, Li et al. 2012)

Eukaryote-prokaryote  (Doolittle, Feng et al. 1990)

Eukaryotic cells (Impossible to identify because Legionella infects and grows in amoebae, protozoa, paramecium, macrophages, and many other eukaryotic cells)

Bacteria Legionella pneumophila

Eukaryote-like regulatory “effector” proteins injected in the course of infecting eukaryotic cells

(Lurie-Weinberger, Gomez-Valero et al. 2010; Gomez-Valero, Rusniok et al. 2011; de la Casa-Esperon 2012; Rolando and Buchrieser 2014; Burstein, Amaro et al. 2016)

Virus-prokaryote

Halovirus

Halobacterium salinarum (Archaea)

B-type DNA polymerase B1

(Filee, Forterre et al. 2002)

Virus-eukaryote

T3/T7 family bacteriophage

Ancestral eukaryote nuclear and mitochondrial genomes

A-type DNA polymerase Gamma of the mitochondrion (Opisthokonts only, metazoa and fungi), mitochondrial single-subunit RNA Polymerase (mt-ssRNAP), nucleus-encoded mitochondrial replicative helicase (all eukaryotes)

(Filee, Forterre et al. 2002; Filee and Forterre 2005; Shutt and Gray 2006)

Double-stranded RNA viruses (totiviruses and partitiviruses)

Eukaryote nuclear genomes (plants, arthropods, fungi, nematodes, and protozoa)

Capsid protein and RNA-dependent RNA polymerases

(Liu, Fu et al. 2010)

Circular single-stranded DNA viruses (geminiviruses, nanoviruses and circoviruses)

Eukaryotic nuclear genomes (plants, fungi, animals and protists)

Replication initiation protein (Rep)-related sequences

(Liu, Fu et al. 2011)

Cellular organisms-virus

Bacteria

Diverse temperate bacteriophages (bacterial viruses capable of insertion into “lysogen” bacterial genome as repressed prophage)

Expressed in lysogens: DNA adenine methylase, DNA cytosine methylase, porin (outer membrane transport), mammalian serum resistance, phage attack resistance, improved survival in Peyer's patches, mammalian cell binding, superoxide dismutase (lysogen more virulent in mice), mammalian cell ruffling and cell invasion, Shiga-like toxin (kills mammalian cells by damaging rRNA)

(Hendrix, Lawrence et al. 2000)

Bacteria (primarily, endosymbionts and parasites), bacteriophages, protists, animals

Nucleocytoplasmic large DNA viruses (NCLDVs), including Poxviruses and Iridoviruses infecting insects and vertebrates, Mimiviruses and Phycodnaviruses infecting amoebae, protists and algae

Small and large subunit rDNAs, DNA polymerase, two subunits of the DNA-dependent RNA polymerase, and two subunits of the ribonucleotide reductase, DNA ligase, dUTPase, serine/threonine kinase, thymidine kinase, ribonucleotide reductase, virus-specific signaling and regulatory domains, ubiquitin signaling; defenses against apoptosis, immune response (the MHC class I, interleukin-10, interleukin-24, interleukin-18, the interferon gamma receptor, and tumor necrosis factor receptor II), including growth factors and potential inhibitors of cytokine signaling, peptidases; glutaredoxin and glutathione peroxidase involved in resistance of cells to oxidative stress.