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Complete Genome Sequence of Methanomassiliicoccus luminyensis, the Largest Genome of a Human-Associated Archaea Species

Journal of Bacteriology

August 2012
194(17):4745

DOI:10.1128/JB.00956-12

Source
PubMed

Authors:

Aurore Gorlas

Université Paris-Saclay

Catherine Robert

Aix-Marseille Université

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The present study describes the complete and annotated genome sequence of Methanomassiliicoccus luminyensis strain B10 (DSM 24529T, CSUR P135), which was isolated from human feces. The 2.6-Mb genome represents the largest genome of a methanogenic euryarchaeon isolated from humans. The genome data of M. luminyensis reveal unique features and horizontal gene transfer events, which might have occurred during its adaptation and/or evolution in the human ecosystem.

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Complete Genome Sequence of Methanomassiliicoccus luminyensis, the

Largest Genome of a Human-Associated Archaea Species

Aurore Gorlas, Catherine Robert, Gregory Gimenez, Michel Drancourt, and Didier Raoult

Unité de Recherche sur les Maladies Infectieuses et Tropicales Emergentes (URMITE), Aix Marseille Université, UMR CNRS 7278, IRD 198, INSERM 1095, Faculté de

Médecine, Marseille, France

The present study describes the complete and annotated genome sequence of Methanomassiliicoccus luminyensis strain B10

(DSM 24529

, CSUR P135), which was isolated from human feces. The 2.6-Mb genome represents the largest genome of a metha-

nogenic euryarchaeon isolated from humans. The genome data of M. luminyensis reveal unique features and horizontal gene

transfer events, which might have occurred during its adaptation and/or evolution in the human ecosystem.

Methanomassiliicoccus luminyensis strain B10 was isolated from hu-

man feces by enrichment culture studies that were conducted to

isolate new human-associated Archaea species (4). The strictly anaerobic

strain B10 grows optimally at 37°C, pH 7.6, with 1% NaCl, and is able to

produce methane by reducing methanol with hydrogen as an electron

donor.

A phylogenetic analysis using 16S rRNA gene sequences showed that

strain B10 is most closely related to the nonmethanogen Aciduliprofun-

dum boonei (4). Strain B10, only the fourth euryarchaeote to be success-

fully cultivated and isolated from humans (5), represents the ﬁrst species

of a novel genus (4).

The complete genome of M. luminyensis was sequenced with a com-

bination of shotgun and 3-kb paired-end libraries using high-through-

put 454 pyrosequencing by 454 Life Sciences (Roche, Boulogne Billan-

court, France). Sequence reads were assembled using a Newbler

assembler (Roche), 26 contigs were generated into one scaffold, and gaps

were closed by PCR on genomic DNA. A preliminary open reading

frame (ORF) prediction was conducted by automated annotation with

Glimmer (http://www.cbcb.umd.edu/software/glimmer/) and RAST

(2). The annotation was manually cured using BLAST and the nr data-

base of NCBI. The CRISPRﬁnder (http://crispr.u-psud.fr/Server/)was

used to detect and identify CRISPR repeat and spacer sequences in the

genome.

The M. luminyensis genome consists of a circular chromosome of

2,637,810 bp (with a high GC content of 60.5%), which is much larger

than the genomes of other methanogenic Archaea isolated from humans:

Methanobrevibacter smithii (1.8 Mb) (10)andMethanosphaera stadt-

manae (1.77 Mb) (6).

The genome of M. luminyensis contains, surprisingly, a single 16S-23S

rRNA cluster (rarely observed for methanogenic Archaea) and two cop-

ies of 5S and 42 tRNA genes. A total of 2,613 ORFs were recovered, and

most of them presumably encode proteins involved in DNA/RNA me-

tabolism, synthesis and degradation of proteins, biosynthesis of nucleo-

tides/amino acids/fatty acids/vitamins and cofactors, and energy metab-

olism.

As for M. stadtmanae,theM. luminyensis genome carries a restricted

methanogenesis pathway, which could explain why M. luminyensis re-

duces only methanol in the presence of H

for methane formation.

Among the proteins involved in DNA metabolism, the DNA replica-

tion machinery of M. luminyensis is strongly conserved with proteins of

archaeal origin such as ORC1/CDC6, RFA, Pri-1, Pri-2, MCM, RFC,

PCNA, FEN, RNase H, DNA polymerase B, and DNA polymerase D

(which is speciﬁc to Euryarchaea)(3). In contrast, the repair system of

M. luminyensis contains proteins of nonarchaeal origin. The genome

contains several genes encoding bacterial proteins such as UvrD helicase

or DinG helicase, suggesting horizontal gene transfers from Bacteria

foundinthegut(1).

Moreover, the M. luminyensis genome contains 3 CRISPR loci and

the associated proteins (Cas), which could confer a resistance against the

intrusion of mobile elements such as viruses and plasmids (9). The dis-

tribution of the CRISPR/Cas systems in Archaea genomes shows an im-

portant horizontal gene transfer from Bacteria driven by mobile elements

(7,8).

These horizontal gene acquisitions from Bacteria might have contrib-

uted to the evolution and adaptation of M. luminyensis to the host niche.

Nucleotide sequence accession numbers. The Methanomassiliicoc-

cus luminyensis strain B10 genome sequence has been deposited in EMBL

under the accession numbers CAJE01000001 to CAJE01000026.

ACKNOWLEDGMENT

This work was funded by Fondation Méditerranée Infection.

We have no conﬂicts of interest to declare.

REFERENCES

1. Aravind L, Walker DR, Koonin EV. 1999. Conserved domains in DNA repair

proteins and evolution of repair systems. Nucleic Acids Res. 27:1223–1242.

2. Aziz RK, et al. 2008. The RAST server: rapid annotations using subsys-

tems technology. BMC Genomics 9:75.

3. Barry ER, Bell SD. 2006. DNA replication in the Archaea. Microbiol. Mol.

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4. Dridi B, Fardeau ML, Ollivier B, Raoult D, Drancourt M. Methano-

massiliicoccus luminyensis, gen. nov., sp. nov., a novel methanogenic Ar-

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5. Dridi B, Raoult D, Drancourt M. 2011. Archaea as emerging organisms

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6. Fricke WF, et al. 2006. The genome sequence of Methanosphaera stadtmanae

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7. Garrett RA, Vestergaard G, Shah SA. 2011. Archaeal CRISPR-based immune

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8. Horvath P, Barrangou R. 2010. CRISPR/Cas, the immune system of

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9. Koonin EV, Marakova KS. 2009. CRISPR-Cas: an adaptative immunity

system in prokaryotes. Biol. Rep. 1:95.

10. Samuel BS, et al. 2007. Genomic and metabolic adaptations of Methanobrevibac-

ter smithii to the human gut. Proc. Natl. Acad. Sci. U. S. A. 104:10643–10648.

Received 31 May 2012 Accepted 12 June 2012

Address correspondence to Didier Raoult, didier.raoult@gmail.com.

doi:10.1128/JB.00956-12

GENOME ANNOUNCEMENT

September 2012 Volume 194 Number 17 Journal of Bacteriology p. 4745 jb.asm.org 4745

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ANAEROBE

In this work, we review the state of knowledge of Archaea associated with the human microbiome. These prokaryotes, initially discovered in extreme environments, were named Archaea because these environments were thought to be the most primitive on Earth. Further research revealed that this terminology is misleading because these organisms were later found in various non-extreme environments, including the human host. Further examination of the human microbiome has enabled the isolation of three archaeal species, Methanobrevibacter smithii, Methanosphaera stadtmanae and Methanobrevibacter oralis, which are associated with oral, intestinal and vaginal mucosae in humans. Moreover, molecular studies including metagenomic analyses detected DNA sequences indicative of the presence of additional methanogenic and non-methanogenic Archaea in the human intestinal tract. All three culturable Archaea are strict anaerobes, although their potential role in human diseases remains to be established. Future research aims to detect and culture additional human mucosa-associated Archaea and to look for their presence in additional human tissues, to establish their role in human infections involving complex flora.

Aravind, L., Walker, D.R. & Koonin, E.V. Conserved domains in DNA repair proteins and evolution of repair systems. Nucleic Acids Res. 27, 1223-1242

Article

Apr 1999

A detailed analysis of protein domains involved in DNA repair was performed by comparing the sequences of the repair proteins from two well-studied model organisms, the bacterium Escherichia coli and yeast Saccharomyces cerevisiae, to the entire sets of protein sequences encoded in completely sequenced genomes of bacteria, archaea and eukaryotes. Previously uncharacterized conserved domains involved in repair were identified, namely four families of nucleases and a family of eukaryotic repair proteins related to the proliferating cell nuclear antigen. In addition, a number of previously undetected occurrences of known conserved domains were detected; for example, a modified helix-hairpin-helix nucleic acid-binding domain in archaeal and eukaryotic RecA homologs. There is a limited repertoire of conserved domains, primarily ATPases and nucleases, nucleic acid-binding domains and adaptor (protein-protein interaction) domains that comprise the repair machinery in all cells, but very few of the repair proteins are represented by orthologs with conserved domain architecture across the three superkingdoms of life. Both the external environment of an organism and the internal environment of the cell, such as the chromatin superstructure in eukaryotes, seem to have a profound effect on the layout of the repair systems. Another factor that apparently has made a major contribution to the composition of the repair machinery is horizontal gene transfer, particularly the invasion of eukaryotic genomes by organellar genes, but also a number of likely transfer events between bacteria and archaea. Several additional general trends in the evolution of repair proteins were noticed; in particular, multiple, independent fusions of helicase and nuclease domains, and independent inactivation of enzymatic domains that apparently retain adaptor or regulatory functions.

Complete Genome Sequence of Methanomassiliicoccus luminyensis, the Largest Genome of a Human-Associated Archaea Species

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Genome Sequence of Weissella cibaria M2, a Potential Probiotic Strain Isolated from the Feces of a G...