Coexistence of Two Different Photosynthetic Operons in Citromicrobium bathyomarinum JL354 As Revealed by Whole-Genome Sequencing

Abstract

Citromicrobium bathyomarinum is a bacteriochlorophyll a-containing aerobic anoxygenic phototrophic bacterium. Here, we report the draft genome sequence of C. bathyomarinum JL354, which was the first C. bathyomarinum strain isolated from a euphotic marine environment. The JL354 genome sequence reveals, for the first time, the coexistence of two different photosynthetic operons in a single strain.Knowledge of aerobic anoxygenic phototrophic bacteria (AAPB) is critical for understanding carbon cycling in the ocean (4, 7), and they have been studied extensively with regard to their abundance and diversity in different marine environments (4, 6, 7, 9, 13, 16, 18, 19). The known marine AAPB species are mainly affiliated with the Alphaproteobacteria (including the alpha-3 and alpha-4 subclusters) and Gammaproteobacteria (3,14). The genus Citromicrobium is one clade of the alpha-4 AAPB subcluster, and it contains only one species, Citromicrobium bathyomarinum. The type strain of C. bathyomarinum, strain JF-1, was isolated from deep-sea hydrothermal vent plume waters (17). Other strains of C. bathyomarinum were isolated at depths from 500 m to 2,379 m (12). All of these habitats are aphotic environments, and the known C. bathyomarinum strains may not play the same ecological role as those AAPB which are in the euphotic zone. Here, we report on the first epipelagic strain of C. bathyomarinum, strain JL354, which was isolated from the surface water of the South China Sea.The C. bathyomarinum JL354 16S rRNA gene shares 99.6% sequence similarity with that of the type strain JF-1. Wholegenome shotgun sequencing was performed on JL354 using 454 pyrosequencing technologies, which produced 207,125 reads and 85,861,877 bp sequences. A total of 201,805 highquality reads were used in assembling the genome to give 26.2-fold coverage of the genome. The complete sequence was analyzed using Glimmer 3.02 (2) for the protein-coding gene, tRNAscan-SE (10) for the tRNA, and RNAmmer (8) for the rRNA. The functions of predicted protein-coding genes were then annotated through comparisons with the databases of NCBI-NR (1), COG (15), and KEGG (5).The C. bathyomarinum JL354 draft genome sequence has a total of 3,273,334 bp (3,401 open reading frames) distributed in 68 contigs with an average GC content of 65.0%. One 16S-23S-5S operon and 45 tRNAs on the draft assembly were identified, as were complete sets of genes for the synthesis of amino acids, nucleotides, and prosthetic groups. In particular, this strain has two different photosynthetic (PS) operons; one is complete, and the other is incomplete. The complete one consists of the typical subclusters puhCBA-lhaA-bchMLHBNF and pufMLAB-bchZYXC-crtFDC, and the incomplete one only has pufLMC-puhCBA. The similarity of the two pufLM gene sequences is less than 70%, and the pufLM gene in the incomplete operon is affiliated with the Gammaproteobacteria group by phylogenetic analysis (3). This is the first report about two different PS operons coexisting in a single strain.A detailed inspection of th...

Diversity of cultivated and metabolically active aerobic anoxygenic phototrophic bacteria along an oligotrophic gradient in the Mediterranean Sea

“…Since these authors were unsuccessful to obtain colonies of C. bathyomarinum offset from hydrothermal vents, they suggest that it may be endemic to deep vent plumes and possibly benefit from hydrothermal effluent components. However, the wide distribution of C. bathyomarinum in the upper waters of the Mediterranean Sea (3 stations within the western basin and the Ionian Sea at the surface and up to 85 m depth) and their occurrence in other surface marine waters (Koblizek et al, 2003;Jiao et al, 2010) does not favor this hypothesis. The frequent isolation of Erythrobacter species is not surprising since Erythrobacter spp.…”

Genome Sequence of Citromicrobium Strain JLT1363, Isolated from the South China Sea

“…In the JLT1363 genome, we found exactly the same genes as those located upstream and downstream of the photosynthetic gene cluster (PGC) of JL354 (6). Their order and direction are the same as well.…”

“…C. bathyomarinum JF-1 and other Citromicrobium spp. were identified as aerobic anoxygenic phototrophic bacteria (AAPB) (6,11,14). We isolated a Citromicrobium sp.…”

Geographic Impact on Genomic Divergence as Revealed by Comparison of Nine Citromicrobial Genomes

“…The genus Citromicrobium, belonging to the order Sphingomonadales in the class Alphaproteobacteria, is a member of the marine AAPB (15)(16)(17). Since the initial isolation of the type species, Citromicrobium bathyomarinum strain JF-1, from deep-sea hydrothermal vent plume waters in the Juan de Fuca Ridge (Pacific Ocean), dozens of Citromicrobium strains were isolated from a depth of 500 to 2,379 m near this region (17,18).…”

“…Genomic analyses showed that members of the genera Citromicrobium and Erythrobacter generally contained the shortest and simplest PGC structures among all known AAPB (16). Analysis of the C. bathyomarinum JL354 genome led to the discovery that two different PGCs could coexist in one bacterium, with one complete cluster and the other cluster incomplete (15,16). Horizontal gene transfer (HGT) was detected to mediate the incomplete PGC acquisition, and multiple mechanisms mediating HGT were also found through studying its genome, including a gene transfer agent (GTA), prophage, integrative conjugative element (ICE), and the type IV secretion system (T4SS).…”