|
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
|
|
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.
|
|