A genomic analysis of the archaeal system Ignicoccus hospitalis-Nanoarchaeum equitans

Mircea Podar; Iain Anderson; Kira S. Makarova; James G. Elkins; Natalia Ivanova; Mark A. Wall; Athanasios Lykidis; Kostantinos Mavromatis; Hui Sun; Matthew E. Hudson; Wenqiong Chen; Cosmin Deciu; Don Hutchison; Jonathan R. Eads; Abraham Anderson; Fillipe Fernandes; Ernest Szeto; Alla Lapidus; Nikos C. Kyrpides; Milton H. Saier; Paul M. Richardson; Reinhard Rachel; Harald Huber; Jonathan A. Eisen; Eugene V. Koonin; Martin Keller; Karl O. Stetter

doi:10.1186/gb-2008-9-11-r158

A genomic analysis of the archaeal system Ignicoccus hospitalis-Nanoarchaeum equitans

Mircea Podar, Iain Anderson, Kira S. Makarova, James G. Elkins, Natalia Ivanova, Mark A. Wall, Athanasios Lykidis, Kostantinos Mavromatis, Hui Sun, Matthew E. Hudson, Wenqiong Chen, Cosmin Deciu, Don Hutchison, Jonathan R. Eads, Abraham Anderson, Fillipe Fernandes, Ernest Szeto, Alla Lapidus, Nikos C. Kyrpides, Milton H. SaierPaul M. Richardson, Reinhard Rachel, Harald Huber, Jonathan A. Eisen, Eugene V. Koonin, Martin Keller, Karl O. Stetter

Synthetic Biology

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Abstract

Background: The relationship between the hyperthermophiles Ignicoccus hospitalis and Nanoarchaeum equitans is the only known example of a specific association between two species of Archaea. Little is known about the mechanisms that enable this relationship. Results: We sequenced the complete genome of I. hospitalis and found it to be the smallest among independent, free-living organisms. A comparative genomic reconstruction suggests that the I. hospitalis lineage has lost most of the genes associated with a heterotrophic metabolism that is characteristic of most of the Crenarchaeota. A streamlined genome is also suggested by a low frequency of paralogs and fragmentation of many operons. However, this process appears to be partially balanced by lateral gene transfer from archaeal and bacterial sources. Conclusions: A combination of genomic and cellular features suggests highly efficient adaptation to the low energy yield of sulfur-hydrogen respiration and efficient inorganic carbon and nitrogen assimilation. Evidence of lateral gene exchange between N. equitans and I. hospitalis indicates that the relationship has impacted both genomes. This association is the simplest symbiotic system known to date and a unique model for studying mechanisms of interspecific relationships at the genomic and metabolic levels.

Original language	English
Article number	R158
Journal	Genome Biology
Volume	9
Issue number	11
DOIs	https://doi.org/10.1186/gb-2008-9-11-r158
State	Published - Nov 10 2008

Funding

We thank Diversa/Verenium Corporation (San Diego, CA), JGI production sequencing group and the Computational Biology Group at Oak Ridge National Laboratory (Oak Ridge, TN) for sequencing and annotation support. MP, JGE and MK were supported by the US Department of Energy, Office of Science, Biological and Environmental Research programs at Oak Ridge National Laboratory (ORNL). ORNL is managed by UT-Battelle, LLC, for the US Department of Energy under contract DE-AC05-00OR22725. Support for sequencing and data analysis was provided by the Joint Genome Institute, the US Department of Energy (IA, NI, AL, KM, HS, ES, AL, NK and PR). Diversa Corporation provided support for MP, MW, WC, CD, DH, JRE, AA and FF. KSM and EVK are supported by the Intramural Research Program of the National Institutes of Health, National Library of Medicine. HH, RR and KOS were supported by grants from the Deutsche Forschungsgemeinschaft.

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Podar, M., Anderson, I., Makarova, K. S., Elkins, J. G., Ivanova, N., Wall, M. A., Lykidis, A., Mavromatis, K., Sun, H., Hudson, M. E., Chen, W., Deciu, C., Hutchison, D., Eads, J. R., Anderson, A., Fernandes, F., Szeto, E., Lapidus, A., Kyrpides, N. C., ... Stetter, K. O. (2008). A genomic analysis of the archaeal system Ignicoccus hospitalis-Nanoarchaeum equitans. Genome Biology, 9(11), Article R158. https://doi.org/10.1186/gb-2008-9-11-r158

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title = "A genomic analysis of the archaeal system Ignicoccus hospitalis-Nanoarchaeum equitans",

abstract = "Background: The relationship between the hyperthermophiles Ignicoccus hospitalis and Nanoarchaeum equitans is the only known example of a specific association between two species of Archaea. Little is known about the mechanisms that enable this relationship. Results: We sequenced the complete genome of I. hospitalis and found it to be the smallest among independent, free-living organisms. A comparative genomic reconstruction suggests that the I. hospitalis lineage has lost most of the genes associated with a heterotrophic metabolism that is characteristic of most of the Crenarchaeota. A streamlined genome is also suggested by a low frequency of paralogs and fragmentation of many operons. However, this process appears to be partially balanced by lateral gene transfer from archaeal and bacterial sources. Conclusions: A combination of genomic and cellular features suggests highly efficient adaptation to the low energy yield of sulfur-hydrogen respiration and efficient inorganic carbon and nitrogen assimilation. Evidence of lateral gene exchange between N. equitans and I. hospitalis indicates that the relationship has impacted both genomes. This association is the simplest symbiotic system known to date and a unique model for studying mechanisms of interspecific relationships at the genomic and metabolic levels.",

author = "Mircea Podar and Iain Anderson and Makarova, {Kira S.} and Elkins, {James G.} and Natalia Ivanova and Wall, {Mark A.} and Athanasios Lykidis and Kostantinos Mavromatis and Hui Sun and Hudson, {Matthew E.} and Wenqiong Chen and Cosmin Deciu and Don Hutchison and Eads, {Jonathan R.} and Abraham Anderson and Fillipe Fernandes and Ernest Szeto and Alla Lapidus and Kyrpides, {Nikos C.} and Saier, {Milton H.} and Richardson, {Paul M.} and Reinhard Rachel and Harald Huber and Eisen, {Jonathan A.} and Koonin, {Eugene V.} and Martin Keller and Stetter, {Karl O.}",

year = "2008",

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doi = "10.1186/gb-2008-9-11-r158",

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Podar, M, Anderson, I, Makarova, KS, Elkins, JG, Ivanova, N, Wall, MA, Lykidis, A, Mavromatis, K, Sun, H, Hudson, ME, Chen, W, Deciu, C, Hutchison, D, Eads, JR, Anderson, A, Fernandes, F, Szeto, E, Lapidus, A, Kyrpides, NC, Saier, MH, Richardson, PM, Rachel, R, Huber, H, Eisen, JA, Koonin, EV, Keller, M & Stetter, KO 2008, 'A genomic analysis of the archaeal system Ignicoccus hospitalis-Nanoarchaeum equitans', Genome Biology, vol. 9, no. 11, R158. https://doi.org/10.1186/gb-2008-9-11-r158

TY - JOUR

T1 - A genomic analysis of the archaeal system Ignicoccus hospitalis-Nanoarchaeum equitans

AU - Podar, Mircea

AU - Anderson, Iain

AU - Makarova, Kira S.

AU - Elkins, James G.

AU - Ivanova, Natalia

AU - Wall, Mark A.

AU - Lykidis, Athanasios

AU - Mavromatis, Kostantinos

AU - Sun, Hui

AU - Hudson, Matthew E.

AU - Chen, Wenqiong

AU - Deciu, Cosmin

AU - Hutchison, Don

AU - Eads, Jonathan R.

AU - Anderson, Abraham

AU - Fernandes, Fillipe

AU - Szeto, Ernest

AU - Lapidus, Alla

AU - Kyrpides, Nikos C.

AU - Saier, Milton H.

AU - Richardson, Paul M.

AU - Rachel, Reinhard

AU - Huber, Harald

AU - Eisen, Jonathan A.

AU - Koonin, Eugene V.

AU - Keller, Martin

AU - Stetter, Karl O.

PY - 2008/11/10

Y1 - 2008/11/10

N2 - Background: The relationship between the hyperthermophiles Ignicoccus hospitalis and Nanoarchaeum equitans is the only known example of a specific association between two species of Archaea. Little is known about the mechanisms that enable this relationship. Results: We sequenced the complete genome of I. hospitalis and found it to be the smallest among independent, free-living organisms. A comparative genomic reconstruction suggests that the I. hospitalis lineage has lost most of the genes associated with a heterotrophic metabolism that is characteristic of most of the Crenarchaeota. A streamlined genome is also suggested by a low frequency of paralogs and fragmentation of many operons. However, this process appears to be partially balanced by lateral gene transfer from archaeal and bacterial sources. Conclusions: A combination of genomic and cellular features suggests highly efficient adaptation to the low energy yield of sulfur-hydrogen respiration and efficient inorganic carbon and nitrogen assimilation. Evidence of lateral gene exchange between N. equitans and I. hospitalis indicates that the relationship has impacted both genomes. This association is the simplest symbiotic system known to date and a unique model for studying mechanisms of interspecific relationships at the genomic and metabolic levels.

AB - Background: The relationship between the hyperthermophiles Ignicoccus hospitalis and Nanoarchaeum equitans is the only known example of a specific association between two species of Archaea. Little is known about the mechanisms that enable this relationship. Results: We sequenced the complete genome of I. hospitalis and found it to be the smallest among independent, free-living organisms. A comparative genomic reconstruction suggests that the I. hospitalis lineage has lost most of the genes associated with a heterotrophic metabolism that is characteristic of most of the Crenarchaeota. A streamlined genome is also suggested by a low frequency of paralogs and fragmentation of many operons. However, this process appears to be partially balanced by lateral gene transfer from archaeal and bacterial sources. Conclusions: A combination of genomic and cellular features suggests highly efficient adaptation to the low energy yield of sulfur-hydrogen respiration and efficient inorganic carbon and nitrogen assimilation. Evidence of lateral gene exchange between N. equitans and I. hospitalis indicates that the relationship has impacted both genomes. This association is the simplest symbiotic system known to date and a unique model for studying mechanisms of interspecific relationships at the genomic and metabolic levels.

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DO - 10.1186/gb-2008-9-11-r158

M3 - Article

C2 - 19000309

AN - SCOPUS:57049130376

SN - 1474-7596

VL - 9

JO - Genome Biology

JF - Genome Biology

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M1 - R158

ER -

A genomic analysis of the archaeal system Ignicoccus hospitalis-Nanoarchaeum equitans

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