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

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Geographic Impact on Genomic Divergence As Revealed by Comparison of Nine Citromicrobial Genomes crossmark Geographic Impact on Genomic Divergence as Revealed by Comparison of Nine Citromicrobial Genomes Qiang Zheng,a Yanting Liu,a Christian Jeanthon,b,c Rui Zhang,a Wenxin Lin,a Jicheng Yao,d Nianzhi Jiaoa State Key Laboratory for Marine Environmental Science, Institute of Marine Microbes and Ecospheres, Xiamen University, Xiamen, People’s Republic of Chinaa; CNRS, UMR 7144, Marine Phototrophic Prokaryotes Team, Station Biologique de Roscoff, Roscoff, Franceb; Sorbonne Universités, UPMC Université Paris 06, UMR 7144, Oceanic Plankton Group, Station Biologique de Roscoff, Roscoff, Francec; Shanghai Personal Biotechnology Limited Company, Shanghai, People’s Republic of Chinad Downloaded from ABSTRACT Aerobic anoxygenic phototrophic bacteria (AAPB) are thought to be important players in oceanic carbon and energy cycling in the euphotic zone of the ocean. The genus Citromicrobium, widely found in oligotrophic oceans, is a member of marine alpha- proteobacterial AAPB. Nine Citromicrobium strains isolated from the South China Sea, the Mediterranean Sea, or the tropical South Atlantic Ocean were found to harbor identical 16S rRNA sequences. The sequencing of their genomes revealed high syn- teny in major regions. Nine genetic islands (GIs) involved mainly in type IV secretion systems, flagellar biosynthesis, prophage, and integrative conjugative elements, were identified by a fine-scale comparative genomics analysis. These GIs played significant http://aem.asm.org/ roles in genomic evolution and divergence. Interestingly, the coexistence of two different photosynthetic gene clusters (PGCs) was not only found in the analyzed genomes but also confirmed, for the first time, to our knowledge, in environmental samples. The prevalence of the coexistence of two different PGCs may suggest an adaptation mechanism for Citromicrobium members to survive in the oceans. Comparison of genomic characteristics (e.g., GIs, average nucleotide identity [ANI], single-nucleotide polymorphisms [SNPs], and phylogeny) revealed that strains within a marine region shared a similar evolutionary history that was distinct from that of strains isolated from other regions (South China Sea versus Mediterranean Sea). Geographic differ- ences are partly responsible for driving the observed genomic divergences and allow microbes to evolve through local adapta- tion. Three Citromicrobium strains isolated from the Mediterranean Sea diverged millions of years ago from other strains and evolved into a novel group. on November 21, 2016 by INIST-CNRS BiblioVie IMPORTANCE Aerobic anoxygenic phototrophic bacteria are a widespread functional group in the upper ocean, and their abundance could be up to 15% of the total heterotrophic bacteria. To date, a great number of studies display AAPB biogeographic distribution pat- terns in the ocean; however, little is understood about the geographic isolation impact on the genome divergence of marine AAPB. In this study, we compare nine Citromicrobium genomes of strains that have identical 16S rRNA sequences but different ocean origins. Our results reveal that strains isolated from the same marine region share a similar evolutionary history that is distinct from that of strains isolated from other regions. These Citromicrobium strains diverged millions of years ago. In addi- tion, the coexistence of two different PGCs is prevalent in the analyzed genomes and in environmental samples. erobic anoxygenic phototrophic bacteria (AAPB) are a wide- structures among all known AAPB (16). Analysis of the C. bathyo- Aspread functional microbial group in the euphotic zone of the marinum JL354 genome led to the discovery that two different ocean and are thought to play important roles in the cycling of PGCs could coexist in one bacterium, with one complete cluster marine carbon and energy (1–10). AAPB can harvest light using and the other cluster incomplete (15, 16). Horizontal gene trans- bacteriochlorophyll a (BChl a) and various carotenoids to form a fer (HGT) was detected to mediate the incomplete PGC acquisi- transmembrane proton gradient for the generation of ATP (1, 11). tion, and multiple mechanisms mediating HGT were also found The photosynthetic process is performed by a series of photosyn- through studying its genome, including a gene transfer agent (GTA), thetic operons, including bch, crt, puf, puh, and some regulatory genes, forming a highly conserved 40- to 50-kb photosynthetic gene cluster (PGC) (12, 13). The heart of anoxygenic photosyn- Received 30 August 2016 Accepted 3 October 2016 thesis is the reaction center, encoded by the puf and puh operons Accepted manuscript posted online 7 October 2016 (14). Citation Zheng Q, Liu Y, Jeanthon C, Zhang R, Lin W, Yao J, Jiao N. 2016. The genus Citromicrobium, belonging to the order Sphin- Geographic impact on genomic divergence as revealed by comparison of nine gomonadales in the class Alphaproteobacteria, is a member of the citromicrobial genomes. Appl Environ Microbiol 82:7205–7216. marine AAPB (15–17). Since the initial isolation of the type spe- doi:10.1128/AEM.02495-16. cies, Citromicrobium bathyomarinum strain JF-1, from deep-sea Editor: M. Kivisaar, University of Tartu Address correspondence to Qiang Zheng, [email protected], or hydrothermal vent plume waters in the Juan de Fuca Ridge (Pa- Nianzhi Jiao, [email protected]. cific Ocean), dozens of Citromicrobium strains were isolated from Supplemental material for this article may be found at http://dx.doi.org/10.1128 a depth of 500 to 2,379 m near this region (17, 18). Genomic /AEM.02495-16. analyses showed that members of the genera Citromicrobium and Copyright © 2016, American Society for Microbiology. All Rights Reserved. Erythrobacter generally contained the shortest and simplest PGC December 2016 Volume 82 Number 24 Applied and Environmental Microbiology aem.asm.org 7205 Zheng et al. TABLE 1 Genome information for the nine strains Genome No. of GϩC No. of No. of No. of No. of Sequencing Strain size (Mb) contigs content (%) genes CDSsa COGs tRNAs coverage (ϫ) Isolation source Accession no. JL31 3.16 22 65.1 3,092 2,960 1,969 45 180 South China Sea LAIH00000000 JL1351 3.16 17 65.1 3,090 2,961 1,981 45 155 South China Sea LAPR00000000 WPS32 3.16 16 64.9 3,056 2,925 1,934 44 250 South China Sea LAPS00000000 JL477 3.26 1 65.0 3,168 3,027 2,004 45 220 South China Sea CP011344 JL354 3.27 68 65.0 3,208 3,137 2,010 45 26 South China Sea ADAE00000000 JL2201 3.27 22 65.1 3,250 3,105 1,975 45 245 South Atlantic Ocean LARQ00000000 RCC1878 3.28 14 64.8 3,194 3,061 1,966 45 205 Mediterranean Sea LBLZ00000000 RCC1885 3.28 14 64.8 3,197 3,063 1,975 45 190 Mediterranean Sea LBLY00000000 Downloaded from RCC1897 3.28 17 64.8 3,192 3,113 1,978 45 440 Mediterranean Sea LUGI01000000 a CDSs, coding sequences. prophage, integrative conjugative element (ICE), and the type IV Genome sequencing and assembly. Whole-genome sequencing of secretion system (T4SS). Citromicrobium species may benefit Citromicrobium sp. strain JL354 was performed by 454 pyrosequencing, as previously reported (15, 16). The genomes of JL31, JL477, JL1351, JL2201, from obtaining genes by HGT to compete and survive in natural http://aem.asm.org/ environments. Additionally, genes encoding xanthorhodopsin, WPS32, RCC1878, RCC1885, and RCC1897 were obtained by an Illumina which is a light-driven proton pump like bacteriorhodopsin (19– MiSeq system. Paired-end reads of average 250-bp length were assembled using the Velvet software (version 2.8) (28). The sequencing coverages 21), but more effective at collecting light, are also found in citro- ϫ ϫ microbial genomes (22, 23). ranged from 155 (JL1351) to 440 (RCC1897). The genome of strain JL477 has been completed, and the other seven genomes each possessed 14 A recent pyrosequencing analysis of pufM genes showed that to 22 contigs (Table 1). Citromicrobium-like AAPB were mainly distributed in the oligo- Gene prediction and annotation. The open reading frames (ORFs) trophic ocean and were relatively more abundant in the upper were analyzed using a combination of Glimmer 3.02 (29) and GeneMark twilight zone (150 to 200 m depth) than in the subsurface waters (30, 31). All predicted ORFs were then annotated using the NCBI Pro- (5 m and 25 m) of the western Pacific Ocean (24). However, in this karyotic Genome Annotation Pipeline (32) and Rapid Annotations using on November 21, 2016 by INIST-CNRS BiblioVie study, no sequences belonging to the incomplete PGC were de- Subsystems Technology (RAST) (33). rRNA identification was performed tected, although the Citromicrobium-like pufM gene belonging to with the RNAmmer 1.2 software (34), and tRNAscan-SE (version 1.21) the complete PGC showed a high relative abundance. was used to identify the tRNA genes (35). Fortunately, a great number of citromicrobial strains have The genomic average nucleotide identity (ANI) was calculated by been isolated from the Mediterranean Sea, the South China Sea, the JSpecies Online Service (http://jspecies.ribohost.com/jspeciesws) and the South Atlantic Ocean (16, 25). The Mediterranean Sea is (36). an almost completely enclosed sea connected with the eastern Core genome and pangenome analyses. Orthologous clusters (OCs) were assigned by grouping all protein sequences from the nine genomes North Atlantic Ocean by the narrow Strait of Gibraltar. The South Ϫ using OrthoMCL based on their sequence similarity (E value Ͻ10 5, China Sea is the largest marginal sea in the western Pacific Ocean, Ͼ50% coverage) (37). The core and pangenomes were analyzed accord- extending from subtropical to tropical zones. The sampled area in ing to the method described by Tettelin et al. (38). The functional proteins the South Atlantic Ocean (13.857°S, 26.018°W) is a region of trop- were classified by comparison with the COG (Clusters of Orthologous ical open oceans. Although a great number of studies showed that Groups) databases (39). microbes displayed biogeographic patterns in the ocean (26, 27), SNP discovery.
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