Genome Sequence of Lentisphaera araneosa HTCC2155^T, the Type Species of the Order Lentisphaerales in the Phylum Lentisphaerae

Abstract

Information on the genome content of deeply branching phyla with very few cultured members is invaluable for expanding understanding of microbial evolution. Lentisphaera araneosa HTCC2155^T was isolated from the Oregon coast using dilution-to-extinction culturing. It is a marine heterotroph found in surface and mesopelagic waters in both the Pacific and Atlantic oceans and has the unusual property of producing a net-like matrix of secreted exopolysaccharide. Here we present the genome sequence of L. araneosa HTCC2155^T, importantly, one of only two sequenced members of the phylum Lentisphaerae.

The phylum Lentisphaerae was designated in 2004 with five isolated organisms, of which two were characterized and served as the basis for the designation of two novel orders (2). The phylum is most closely related to Verrucomicrobia, Chlamydiae, Planctomycetes, and the candidate division OP3; these phyla make up a recently designated monophyletic superphylum, PVC (11, 15). Within the phylum Lentisphaerae, clone sequences have been obtained from a variety of environments (2 [and references therein], 16). Isolated from surface waters off the Oregon coast by dilution-to-extinction culturing (3, 13), two organisms with identical 16S rRNA gene sequences were named Lentisphaera araneosa and make up the order Lentisphaerales (2). Here we present the genome sequence of the type strain, L. araneosa HTCC2155^T.

L. araneosa HTCC2155^T was isolated from seawater samples collected at 10 m using low-nutrient heterotrophic medium (2). The genome sequence was determined by shotgun sequencing at the J. Craig Venter Institute as part of the Moore Foundation Microbial Genome Sequencing Project (http://www.moore.org/microgenome). This draft unclosed genome, consisting of 81 contigs (ABCK01000001 to ABCK01000081), was analyzed with the GenDB program (7) at the Center for Genome Research and Biocomputing at Oregon State University, similarly to Previous analyses (9, 10) and through the Joint Genome Institute IMG/M website (http://img.jgi.doe.gov/cgi-bin/pub/main.cgi) (5). The draft genome comprises 5,173 open reading frames (ORFs), 6,023,180 bases, with a G+C content of 40.95%. Forty-nine percent of these ORFs have predicted functions. The genome is predicted to contain 55 tRNA genes, 5 5S rRNA genes, 3 16S rRNA genes, and 1 23S rRNA gene. There are putative genes for a complete tricarboxylic acid cycle, glycolysis, the pentose phosphate pathway, and amino acid synthesis.

Notably, the L. araneosa genome contains 267 putative sulfatases. Since the primary described role of sulfatases is liberating sulfur from sulfate esters during sulfate deprivation (reference 14 and references therein), such a quantity of these genes in this organism is surprising, given the abundance of sulfate in marine environments. The genome of the marine planctomycete Pirellula sp. strain 1 contained 110 putative sulfatases which the authors hypothesized were involved in sulfur scavenging from marine snow (4).

L. araneosa was so named because the exopolysaccharide (EPS) secreted during growth forms a web-like matrix between cells. The genome contains several putative genes connected with EPS production—22 predicted glycosyltransferases, several of which are located two genes downstream from putative UDP-N-acetylglucosamine 2-epimerases (epsC homologs) in eps gene cluster-like configurations (12, 14). EPS production has been connected to psychrotolerance in several strains (1, 6, 8) and with increased pressure (6). The highest relative abundances of L. araneosa were measured in upper mesopelagic waters off the Oregon coast and at the Bermuda Atlantic Time Series station (2). We hypothesize that predicted EPS production genes confer increased fitness on L. araneosa in mid-ocean environments by stimulating the formation of aggregates (“marine snow”) or by interfering with predation.

Nucleotide sequence accession number.

The draft genome sequence of L. araneosa HTCC2155^T is available in GenBank under accession number ABCK00000000 and also in the Marine Microbial Genomics database at Oregon State University (http://bioinfo.cgrb.oregonstate.edu/microbes/).