scieee Science in your language
[en] (orig)

Horizontal gene transfer in asgard archaea

Abstract

Asgard archaea are considered to be the closest prokaryotic relative of eukaryotes [1]. They harbor many of what were previously thought to be eukaryote-exclusive proteins [1], including actin and actin-related proteins [2], and the presence of an actin cytoskeleton in particular has been proven in an isolated Lokiarchaeum [3]. As such, they are a key player in the debate surrounding the origin of eukaryotes (a process called eukaryogenesis) [4]. Being prokaryotes, the genome evolution of the Asgard Archaea is likely to have been shaped in no small part by Horizontal Gene Transfer (HGT), that is, the transfer of genetic material between organisms that are not bound by a parentoffspring relationship [5]. These transferred genes often encode for proteins that are beneficial for the cell and allow for adaptation to new niches [6]. In this work, we aim to unveil the fraction of the Asgard protein repertoire that stems from horizontal transfer events, by applying a HGT detection pipeline that combines homologybased and phylogeny-based methods. By analyzing the functional categories and putative donors of these genes, we hope to understand more about the evolution of Asgard archaeal genomes, so that we can employ this knowledge to shed light on the putative ecology and relationships of the archaeal partner of the symbiosis that would give rise to eukaryotic cells.

Read accessible full text

Horizontal gene transfer in asgard archaea

Author: Manzano-Morales, Saioa,Gabaldón, Toni
Publisher: Barcelona Supercomputing Center
Year: 2023
Source: https://upcommons.upc.edu/bitstream/2117/428134/1/SODS2023-24.pdf
Ho izon al Gene T ans e in Asga d A chaea
Saioa Manzano-Mo ales∗†, Toni Gabald´
on∗†‡
∗Ba celona Supe compu ing Cen e , Ba celona, Spain
†Ins i u e o Resea ch in Biomedicine (IRB Ba celona), The Ba celona Ins i u e o Science and Technology, Ba celona, Spain
‡Ins i uci´
on Ca alana de In es igaci´
on y Es udios A anzados, Ba celona, Spain
E-mail: [email p o ec ed], [email p o ec ed]
Keywo ds—Ho izon al Gene T ans e , Asga d A chaea, Re icu-
la e e olu ion, euka yogenesis.
I. EXTENDED ABSTRACT
Asga d a chaea a e conside ed o be he closes p oka yo ic
ela i e o euka yo es [1]. They ha bo many o wha we e
p e iously hough o be euka yo e-exclusi e p o eins [1],
including ac in and ac in- ela ed p o eins [2], and he p esence
o an ac in cy oskele on in pa icula has been p o en in an
isola ed Lokia chaeum [3]. As such, hey a e a key playe
in he deba e su ounding he o igin o euka yo es (a p ocess
called euka yogenesis) [4].
Being p oka yo es, he genome e olu ion o he Asga d
A chaea is likely o ha e been shaped in no small pa by
Ho izon al Gene T ans e (HGT), ha is, he ans e o gene ic
ma e ial be ween o ganisms ha a e no bound by a pa en -
o sp ing ela ionship [5]. These ans e ed genes o en encode
o p o eins ha a e bene icial o he cell and allow o
adap a ion o new niches [6].
In his wo k, we aim o un eil he ac ion o he Asga d
p o ein epe oi e ha s ems om ho izon al ans e e en s, by
applying a HGT de ec ion pipeline ha combines homology-
based and phylogeny-based me hods. By analyzing he unc-
ional ca ego ies and pu a i e dono s o hese genes, we hope
o unde s and mo e abou he e olu ion o Asga d a chaeal
genomes, so ha we can employ his knowledge o shed
ligh on he pu a i e ecology and ela ionships o he a chaeal
pa ne o he symbiosis ha would gi e ise o euka yo ic
cells.
A. HGT de ec ion pipeline
The genomic sequences and p o ein p edic ions o he
cul u ed isola es Candida us P ome heoa chaeum syn oph-
icum MK-D1 [7] (assembly accession GCF-008000775.1) and
Candida us Lokia chaeum ossi e um/Lokia chaeum sp. B-35
[3] (GenBank code CP104013.1) we e downloaded om NCBI
Assembly and NCBI Nucleo ide/P o ein, espec i ely.
We pe o med a simila i y sea ch wi h BLAST 2.11.0 [8]
o he p o eomes agains a cus om-made da abase comp ised
o all he species ep esen a i es o he Genome Taxonomy
Da abase [9] species ep esen a i es and p o eomes om a
cu a ed se o euka yo es, o ob ain a su icien ly ep esen a i e
sampling o p o ein sequences ac oss he T ee o Li e.
We pa sed he BLAST esul s wi h HGTec o [10], which
sys ema ically analyzes BLAST esul s looking o hi dis ibu-
ion pa e ns incong uen wi h a e ical e olu ion, gi en a se-
ies o hie a chically de ined e olu iona y ca ego ies. This s ep
Fig. 1. HGT de ec ion pipeline
iden i ied pu a i e ho izon ally- ans e ed genes: o hose,
we e ie ed he bes 150 hi s and econs uc ed a gene ee
ollowing he algo i hm implemen ed o PhylomeDB [11]. We
u he analyzed he esul ing gene ees wi h Abaccus [12],
which iden i ies axonomical “jumps” in gene ees ha do
no ollow he species ee and he e o e u he helps disce n
pu a i e HGT e en s. Las ly, we pe o med a manual cu a ion
wi h an e e3-based in-house sc ip [13] o u he il e ou
alse posi i es and o assess he accep o and dono clades.
B. Resul s
Table I displays he numbe o pu a i ely ans e ed genes
pe s ep in he pipeline and o ganism. 9.39% and 6.94% o
he p o ein con en o Ca. Lokia chaeum ossi e um and Ca.
P ome heoa chaeum syn ophicum, espec i ely, is o bac e ial
o igin.
The ans e e en s ha e occu ed o e a se ies o ime-
poin s ac oss he Asga d lineage 2: om genus-le el o
ans e s ha p ecede he di e si ica ion o he Loki lineage.
In e es ingly, he e is a high deg ee o pa aphyly, wi h many
ins ances o he Asga d lineage o ming wo (o mo e) clades:
one ha b anches close o A chaea ( he e o e, likely a copy o
e ical inhe i ance) and one ha b anches close o a bac e ial
clade ( he e o e, a likely ans e ). This implies some deg ee
TABLE I. NUMBER OF HORIZONTALLY TRANSFERRED GENES)
O ganism P o . HGTec o Abaccus HGTs
Ca. L. ossi e um 5119 717 513 481 (442)
Ca. P. syn ophicum 3890 432 359 270 (256)
ossi e um
syn ophicum
Lokia chaeum AMARA-1 CR-4 Lokia chaeia Asga da chaeo a P ome heoa chaeum AMARA-1 CR-4 Lokia chaeia Asga da chaeo a
0
30
60
90
120
T ans e pa ne
Numbe o HGT ees
monophyly_lineage
False
T ue
A
ossi e um
syn ophicum
Lokia chaeum AMARA-1 CR-4 Lokia chaeia Asga da chaeo a P ome heoa chaeum AMARA-1 CR-4 Lokia chaeia Asga da chaeo a
0
30
60
90
120
T ans e pa ne
Numbe o HGT ees
monophyly_Asga d
False
T ue
B
Fig. 2. Ba plo displaying he numbe o ees pe ans e accep o . (A) Monophyly o he accep o lineage. (B) Monophyly o he Asga d a chaea.
o subs i u ion o e ically-inhe i ed copies by ans e ed
ones, and a co-exis ence o bo h sou ces ac oss he Asga d
clade. Independen ans e e en s also canno be uled ou .
These ans e s come om a wide a ange o dono phyla,
wi h p ominen dono s being Fi micu es and Chlo o lexo a,
ollowed by P o eobac e ia, Spi ochaeo a, Desul obac e io a
and Bac e oido a. The con ibu ion o Desul obac e o a is
pa icula ly in e es ing, as sul a e- educing bac e ia a e known
syn ophic pa ne s o hese Asga d a chaea. The con ibu ion
o Anae olineae wi hin Chlo o lexo a is also non- i ial, since
his lineage is known o inhabi ma ine sedimen s, a habi a
whe e hese Lokia chaeia ha e been sampled.
We ound ins ances o bo h Bac e ia- o-Asga d and Asga d-
o-Bac e ia ans e , implying bidi ec ional low be ween ans-
e pa ne s.
T ans e ed genes seem o be en iched in me abolic unc-
ions, mainly ela ed o lipid and amino acid me abolism, unc-
ions ha seem cen al o he unc ions o he cell. They seem
o mainly be componen s o he memb ane (GO:0016021), and
he e is a high deg ee o o e lap be ween bo h Lokia chaeia.
C. Conclusion
In his s udy, we obse e HGT e en s o be widesp ead
ac oss Asga d e olu ion, cons i u ing a con inuous low o
ans e ed genes a di e en poin s in he di e si ica ion o
hese a chaea, and coming om a a ie y o dono s, some o
which can be linked by a me abolic o ecologic ela ionship.
II. ACKNOWLEDGMENT
This esea ch was suppo ed by Go don and Be y Moo e
Founda ion (G an GBMF9742).
REFERENCES
[1] K. Za emba-Niedzwiedzka e al., “Asga d a chaea illumina e he o igin
o euka yo ic cellula complexi y,” Na u e, ol. 541, no. 7637, pp. 353–
358, Jan. 2017.
[2] C. Akıl and R. C. Robinson, “Genomes o asga d a chaea encode
p o ilins ha egula e ac in,” Na u e, ol. 562, no. 7727, pp. 439–443,
Oc . 2018.
[3] T. Rod igues-Oli ei a e al., “Ac in cy oskele on and complex cell
a chi ec u e in an asga d a chaeon,” Na u e, ol. 613, no. 7943, pp.
332–339, Jan. 2023.
[4] E. V. Koonin, “The o igin and ea ly e olu ion o euka yo es in he ligh
o phylogenomics,” Genome Biol., ol. 11, no. 5, p. 209, May 2010.
[5] W. F. Dooli le, “La e al genomics,” T ends Cell Biol., ol. 9, no. 12,
pp. M5–8, Dec. 1999.
[6] J. J. Powe e al., “Adap i e e olu ion o hyb id bac e ia by ho izon al
gene ans e ,” P oc. Na l. Acad. Sci. U. S. A., ol. 118, no. 10, Ma .
2021.
[7] H. Imachi e al., “Isola ion o an a chaeon a he p oka yo e-euka yo e
in e ace,” Na u e, ol. 577, no. 7791, pp. 519–525, Jan. 2020.
[8] S. F. Al schul e al., “Basic local alignmen sea ch ool,” Jou nal o
Molecula Biology, ol. 215, no. 3, pp. 403–410, Oc . 1990. [Online].
A ailable: h ps://doi.o g/10.1016/s0022-2836(05)80360-2
[9] D. H. Pa ks e al., “GTDB: an ongoing census o bac e ial and a chaeal
di e si y h ough a phylogene ically consis en , ank no malized and
comple e genome-based axonomy,” Nucleic Acids Res., ol. 50, no. D1,
pp. D785–D794, Jan. 2022.
[10] Q. Zhu e al., “HGTec o : an au oma ed me hod acili a ing genome-
wide disco e y o pu a i e ho izon al gene ans e s,” BMC Genomics,
ol. 15, p. 717, Aug. 2014.
[11] D. Fuen es e al., “PhylomeDB 5: an expanding eposi o y o genome-
wide ca alogues o anno a ed gene phylogenies,” Nucleic Acids Res.,
ol. 50, no. D1, pp. D1062–D1068, Jan. 2022.
[12] M. A. Na anjo-O ´
ız e al., “Widesp ead in e - and in a-domain ho -
izon al gene ans e o d-amino acid me abolism enzymes in euka y-
o es,” F on . Mic obiol., ol. 7, p. 2001, Dec. 2016.
[13] J. Hue a-Cepas e al., “ETE 3: Recons uc ion, analysis, and isual-
iza ion o phylogenomic da a,” Mol. Biol. E ol., ol. 33, no. 6, pp.
1635–1638, Jun. 2016.
Saioa Manzano-Mo ales ecei ed his BSc deg ee
in Biochemis y and Molecula Biology om he
Uni e si y o he Basque Coun y (UPV-EHU), Spain
in 2019. She hen comple ed he MSc deg ee in
Compu a ional Biology om he Poli echnical Uni-
e si y o Mad id, Spain in 2021. A e a b ie
in e nship in he CIB Ma ga i a Salas (CSIC), she
has been wi h he Compa a i e Genomics g oup o
Ba celona Supe compu ing Cen e (BSC), whe e she
is de eloping he PhD.