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. 2010 Nov 9;107(45):19508-13.
doi: 10.1073/pnas.1007615107. Epub 2010 Oct 25.

Giant virus with a remarkable complement of genes infects marine zooplankton

Matthias G Fischer  1 , Michael J Allen, William H Wilson, Curtis A Suttle
Affiliations

Giant virus with a remarkable complement of genes infects marine zooplankton

Matthias G Fischer et al. Proc Natl Acad Sci U S A. .

Abstract

As major consumers of heterotrophic bacteria and phytoplankton, microzooplankton are a critical link in aquatic foodwebs. Here, we show that a major marine microflagellate grazer is infected by a giant virus, Cafeteria roenbergensis virus (CroV), which has the largest genome of any described marine virus (≈730 kb of double-stranded DNA). The central 618-kb coding part of this AT-rich genome contains 544 predicted protein-coding genes; putative early and late promoter motifs have been detected and assigned to 191 and 72 of them, respectively, and at least 274 genes were expressed during infection. The diverse coding potential of CroV includes predicted translation factors, DNA repair enzymes such as DNA mismatch repair protein MutS and two photolyases, multiple ubiquitin pathway components, four intein elements, and 22 tRNAs. Many genes including isoleucyl-tRNA synthetase, eIF-2γ, and an Elp3-like histone acetyltransferase are usually not found in viruses. We also discovered a 38-kb genomic region of putative bacterial origin, which encodes several predicted carbohydrate metabolizing enzymes, including an entire pathway for the biosynthesis of 3-deoxy-d-manno-octulosonate, a key component of the outer membrane in Gram-negative bacteria. Phylogenetic analysis indicates that CroV is a nucleocytoplasmic large DNA virus, with Acanthamoeba polyphaga mimivirus as its closest relative, although less than one-third of the genes of CroV have homologs in Mimivirus. CroV is a highly complex marine virus and the only virus studied in genetic detail that infects one of the major groups of predators in the oceans.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
Genome diagram of CroV. Genome coordinates are given in kbs. Nested circles from outermost to innermost correspond to (i) predicted CDSs on forward strand and (ii) reverse strand; (iii) expression data for CDSs on forward strand and (iv) reverse strand; (v) gene promoter type for CDSs on forward strand and (vi) reverse strand; (vii) location of repetitive DNA elements; (viii) GC content plotted relative to the genomic mean of 23.35% G+C. The speckled regions at the chromosome ends are not drawn to scale and indicate terminal repeats for which no sequence information is available. A 38-kb genomic segment of putative bacterial origin is shaded orange.
Fig. 2.
Fig. 2.
Early and late gene promoter motifs in CroV. (A) Sequence logos depicting the consensus sequence for putative early (AAAAATTGA) and late (TCTA) promoter motifs. Pie charts show gene expression data for those CDSs that contained the respective motifs within their immediate 5′ upstream regions. The majority of CDSs associated with the AAAAATTGA motif were first seen expressed at 0–3 h p.i., whereas transcripts for most of the TCTA-associated CDSs were not detected until 6 h p.i. or later. (B) Positional distribution of the two motifs relative to the predicted start codon. A narrow distribution with a peak around position −40 is observed for the AAAAATTGA motif (n = 191). The TCTA motif (n = 72) occurs preferentially at position −13 to −21. The search for this motif was restricted to the upstream 30-nt region.
Fig. 3.
Fig. 3.
The predicted KDO biosynthesis pathway in CroV. (A) Schematic of the three enzymatic steps that transform d-ribulose 5-phosphate into KDO. Activation of KDO to CMP-KDO is catalyzed by the cytidylyltransferase CKS. PEP, phosphoenolpyruvate. (B) Organization of the predicted KDO gene cluster (crov265–crov267) in the CroV genome. All three CDSs are predicted bifunctional enzymes. Genome coordinates are given. DMKMT, demethylmenaquinone methyltransferase; TDP-DHMT, dTDP-6-deoxy-l-hexose 3-O-methyltransferase; CMP-NeuAcS, N-acylneuraminate cytidylyltransferase.
Fig. 4.
Fig. 4.
Phylogenetic reconstruction of NCLDV members. The unrooted Bayesian Inference (BI) tree was generated from a 263-aa alignment of conserved regions of DNA polymerase B. Intein insertions were removed before alignment. Nodes are labeled with BI posterior probabilities and maximum likelihood bootstrap values (500 replicates). Abbreviations and accession numbers (GenBank unless stated otherwise) are as follows: ACMV, Acanthamoeba castellanii mamavirus, from ref. ; AMV, Amsacta moorei entomopoxvirus, NP_064832; APMV, A. polyphaga mimivirus, YP_142676; ASFV, African swine fever virus, NP_042783; ATCV-1, Acanthocystis turfacea chlorella virus 1, YP_001427279; CeV-01, C. ericina virus 01, ABU23716; CIV, Chilo iridiscent virus, NP_149500; CroV, C. roenbergensis virus; DpAV4, Diadromus pulchellus ascovirus 4a, CAC19127; EhV-86, E. huxleyi virus 86, YP_293784; ESV-1, Ectocarpus siliculosus virus 1, NP_077578; FirrV-1, Feldmannia irregularis virus 1, AAR26842; FPV, Fowlpox virus, NP_039057; FV3, Frog virus 3, YP_031639; HaV-01, H. akashiwo virus 01, BAE06251; HcDNAV, Heterocapsa circularisquama DNA virus, DDBJ accession no. AB522601; HvAV3, Heliothis virescens ascovirus 3e, YP_001110854; IIV-3, Invertebrate iridiscent virus 3, YP_654692; ISKNV, Infectious spleen and kidney necrosis virus, NP_612241; LDV, Lymphocystis disease virus, YP_073706; MCV, Molluscum contagiosum virus, AAL40129; MSV, Melanoplus sanguinipes entomopoxvirus, NP_048107; MV, Marseillevirus, MAR_ORF329, GU071086; OtV5, Ostreococcus tauri virus 5, YP_001648316; PBCV-1, P. bursarium chlorella virus 1, NP_048532; PoV-01, P. orientalis virus 01, ABU23717; PpV-01, P. pouchetti virus 01, ABU23718; TnAV2, Trichoplusia ni ascovirus 2c, YP_803224; VV, Vaccinia virus, AAA98419.
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