Unique mobile elements and scalable gene flow at the prokaryote-eukaryote boundary revealed by circularized Asgard archaea genomes
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作者:
Wu, Fabai
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CALTECH, Div Geol & Planetary Sci, Pasadena, CA 91125 USA
CALTECH, Div Biol & Biol Engn, Pasadena, CA 91125 USACALTECH, Div Geol & Planetary Sci, Pasadena, CA 91125 USA
Wu, Fabai
[1
,2
]
Speth, Daan R.
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CALTECH, Div Geol & Planetary Sci, Pasadena, CA 91125 USA
CALTECH, Div Biol & Biol Engn, Pasadena, CA 91125 USACALTECH, Div Geol & Planetary Sci, Pasadena, CA 91125 USA
Speth, Daan R.
[1
,2
]
Philosof, Alon
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CALTECH, Div Geol & Planetary Sci, Pasadena, CA 91125 USACALTECH, Div Geol & Planetary Sci, Pasadena, CA 91125 USA
Philosof, Alon
[1
]
Cremiere, Antoine
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CALTECH, Div Geol & Planetary Sci, Pasadena, CA 91125 USACALTECH, Div Geol & Planetary Sci, Pasadena, CA 91125 USA
Cremiere, Antoine
[1
]
Narayanan, Aditi
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CALTECH, Div Biol & Biol Engn, Pasadena, CA 91125 USACALTECH, Div Geol & Planetary Sci, Pasadena, CA 91125 USA
Narayanan, Aditi
[2
]
Barco, Roman A.
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Univ Southern Calif, Dept Earth Sci, Los Angeles, CA USACALTECH, Div Geol & Planetary Sci, Pasadena, CA 91125 USA
Barco, Roman A.
[3
]
Connon, Stephanie A.
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CALTECH, Div Geol & Planetary Sci, Pasadena, CA 91125 USACALTECH, Div Geol & Planetary Sci, Pasadena, CA 91125 USA
Connon, Stephanie A.
[1
]
Amend, Jan P.
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Univ Southern Calif, Dept Earth Sci, Los Angeles, CA USA
Univ Southern Calif, Dept Biol Sci, Los Angeles, CA USACALTECH, Div Geol & Planetary Sci, Pasadena, CA 91125 USA
Amend, Jan P.
[3
,4
]
Antoshechkin, Igor A.
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CALTECH, Div Biol & Biol Engn, Pasadena, CA 91125 USACALTECH, Div Geol & Planetary Sci, Pasadena, CA 91125 USA
Antoshechkin, Igor A.
[2
]
Orphan, Victoria J.
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CALTECH, Div Geol & Planetary Sci, Pasadena, CA 91125 USA
CALTECH, Div Biol & Biol Engn, Pasadena, CA 91125 USACALTECH, Div Geol & Planetary Sci, Pasadena, CA 91125 USA
Orphan, Victoria J.
[1
,2
]
机构:
[1] CALTECH, Div Geol & Planetary Sci, Pasadena, CA 91125 USA
[2] CALTECH, Div Biol & Biol Engn, Pasadena, CA 91125 USA
[3] Univ Southern Calif, Dept Earth Sci, Los Angeles, CA USA
[4] Univ Southern Calif, Dept Biol Sci, Los Angeles, CA USA
Eukaryotic genomes are known to have garnered innovations from both archaeal and bacterial domains but the sequence of events that led to the complex gene repertoire of eukaryotes is largely unresolved. Here, through the enrichment of hydrothermal vent microorganisms, we recovered two circularized genomes of Heimdallarchaeum species that belong to an Asgard archaea clade phylogenetically closest to eukaryotes. These genomes reveal diverse mobile elements, including an integrative viral genome that bidirectionally replicates in a circular form and aloposons, transposons that encode the 5,000 amino acid-sized proteins Otus and Ephialtes. Heimdallaechaeal mobile elements have garnered various genes from bacteria and bacteriophages, likely playing a role in shuffling functions across domains. The number of archaea- and bacteria-related genes follow strikingly different scaling laws in Asgard archaea, exhibiting a genome size-dependent ratio and a functional division resembling the bacteria- and archaea-derived gene repertoire across eukaryotes. Bacterial gene import has thus likely been a continuous process unaltered by eukaryogenesis and scaled up through genome expansion. Our data further highlight the importance of viewing eukaryogenesis in a pan-Asgard context, which led to the proposal of a conceptual framework, that is, the Heimdall nucleation-decentralized innovation-hierarchical import model that accounts for the emergence of eukaryotic complexity. The recovery of two circularized genomes of the Heimdallarchaeum species from hydrothermal vent enrichment cultures reveals that these Asgard archaea carry diverse mobile genetic elements, such as an integrative viral genome and aloposons. These mobile genetic elements contain several bacteria- and phage-derived genes, modulating the shuffling of information between bacteria and archaea, and potentially influencing eukaryogenesis.