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Qt6506g5sk.Pdf UC Irvine UC Irvine Previously Published Works Title Genomic islands and the ecology and evolution of Prochlorococcus. Permalink https://escholarship.org/uc/item/6506g5sk Journal Science (New York, N.Y.), 311(5768) ISSN 0036-8075 Authors Coleman, Maureen L Sullivan, Matthew B Martiny, Adam C et al. Publication Date 2006-03-01 DOI 10.1126/science.1122050 License https://creativecommons.org/licenses/by/4.0/ 4.0 Peer reviewed eScholarship.org Powered by the California Digital Library University of California REPORTS ond, the 3¶ end of tRNA-proline, which flanks Genomic Islands and the Ecology and ISL3 in both genomes, is repeated 13 times in MIT9312-ISL3 (Fig. 2A) and three times in Evolution of Prochlorococcus MED4-ISL3 (fig. S2), suggesting repeated remodeling of this island. Third, some of the Maureen L. Coleman,1 Matthew B. Sullivan,1 Adam C. Martiny,1 Claudia Steglich,1* genes found in a particular island in MED4 are Kerrie Barry,2 Edward F. DeLong,1 Sallie W. Chisholm1† found in a different island in MIT9312 (Fig. 1), a rearrangement that may have been mediated by a Prochlorococcus ecotypes are a useful system for exploring the origin and function of diversity 48–base pair sequence element we call PRE1 among closely related microbes. The genetic variability between phenotypically distinct strains (Prochlorococcus repeat element 1; fig. S3); that differ by less that 1% in 16S ribosomal RNA sequences occurs mostly in genomic islands. portions of PRE1 are repeated, almost exclu- Island genes appear to have been acquired in part by phage-mediated lateral gene transfer, and sively in islands, 13 times in MED4 (fig. S2), and some are differentially expressed under light and nutrient stress. Furthermore, genome fragments 9 times in MIT9312 (Fig. 2A). Finally, up to 80% directly recovered from ocean ecosystems indicate that these islands are variable among co- of the genes in any given MIT9312 island are occurring Prochlorococcus cells. Genomic islands in this free-living photoautotroph share features most similar to the genes of noncyanobacterial with pathogenicity islands of parasitic bacteria, suggesting a general mechanism for niche organisms including phage, Eukarya, and Archaea, differentiation in microbial species. consistent with the recent observation that hor- izontally acquired genomic islands reflect a losely related bacterial isolates often con- except for a large inversion around the repli- gene pool that differs from that of the core ge- tain remarkable genomic diversity (1, 2). cation terminus (Fig. 1). The average G þ C nome (14). CAlthough its functional consequences content is similar in both genomes (31%), and It is likely that phage, which often carry have been described in a few model heterotro- the median sequence identity of the shared host genes (15, 16), mediate some of the island- phic microbes (3), little is known about genomic genes is 78%, surprisingly low for strains so associated lateral gene transfer, and the hli gene microdiversity in the microbial phototrophs that similar at the rRNA locus (11). For most genes, family in particular appears to have undergone dominate aquatic ecosystems. The marine cya- synonymous sites are saturated and protein se- repeated phage-host gene exchange (16). Of the nobacterium Prochlorococcus offers a useful quence identity is low (median 80%); this is 24 hli genes in MIT9312, 18 are found in the system for studying this issue, because they are likely a function of high mutation rates, given five major islands or their flanking regions. All globally abundant, have very simple growth re- that HL Prochlorococcus lack several impor- 18 belong to the multicopy and sporadically quirements, have a very compact genome E1.7 tant DNA-repair enzymes (10, 12). distributed group that includes phage copies to 2.4 megabases (Mb)^, and live in a well-mixed The strain-specific genes between MED4 (Fig. 2A) and is well differentiated from wide- habitat. Although the latter appears to offer few and MIT9312 (236 in MIT9312 and 139 in spread single-copy hli genes found in cyano- opportunities for niche differentiation, Prochlo- MED4) occur primarily (80 and 74%, respec- bacteria (16). Other phagelike genes in islands rococcus populations consist of multiple coex- tively) in five major islands (Fig. 1). Thus, these include an integrase, DNA methylases, a second isting ecotypes (4), whose relative abundances genomes have a mosaic structure similar to that phoH, a MarR-family transcriptional regulator, a vary markedly along gradients of light, temper- of Escherichia coli genomes (1),thoughona putative hemagglutinin neuraminidase, and an ature, and nutrients (5–9). Even two high-light smaller scale. The islands are located in the endonuclease (15), further supporting a link be- adapted (HL) ecotypes, whose type strains (MED4 same position in both genomes, implying that tween phage and island dynamics. and MIT9312) differ by only 0.8% in 16S ribo- they are hotspots for recombination, and the Many island genes in the two strains ap- somal RNA (rRNA) sequence, have substantial- length of island genes is similar to the whole- pear to encode functions related to physiolog- ly different distributions in the wild (5–9). genome average, suggesting that they are not ical stress and nutrient uptake and thus may be Although whole-genome comparisons be- degraded. We hypothesize that these islands important in the high-light, low-nutrient surface tween the most distantly related Prochlorococ- arose via lateral gene transfer and continually un- waters dominated by HL Prochlorococcus. cus isolates (97.9% 16S rRNA identity) have dergo rearrangement, on the basis of a number of ISL2 and ISL5 in MIT9312, for example, en- revealed the gross signatures of this niche differ- characteristics. First, three islands are associated code 12 of the 24 hli genes, known to be im- entiation (10), important insights into the evolution with tRNA genes (fig. S1), which are common portant under a variety of stress conditions (17); of diversity in this group likely lie in comparisons integration sites for mobile elements (13). Sec- they also encode two outer-membrane transport between very closely related strains, and between coexisting genomes from wild populations. Thus, we compared the complete genomes of the type strains, MED4 and MIT9312, that represent the ISL1 ISL2 ISL3 ISL4 ISL5 Fig. 1. Whole-genome alignment two HL clades, and we analyzed genome frag- showing the positions of orthologous ments from wild cells belonging to these clades 1600 genes in MED4 and MIT9312. from the Atlantic and Pacific oceans. ISL5 Strain-specific genes appear on the The 1574 shared genes of MED4 and ISL4 axes. The locations of five major is- MIT9312 have conserved order and orientation, n 1200 ISL3 lands defined by whole-genome e g 25 alignment ( )areshaded. 2 1 1 3 Massachusetts Institute of Technology, Department of Civil 9 T 800 and Environmental Engineering, 15 Vassar Street, Cam- I Me ISL2 bridge, MA 02139, USA. 2U.S. Department of Energy Joint Genome Institute, Production Genomics Facility, Walnut Creek, CA 94598, USA. 400 ISL1 *Present address: University Freiburg, Department of Biology II/Experimental Bioinformatics, Scha¨nzlestrasse 1, D-79104 Freiburg, Germany. 0 †To whom correspondence should be addressed. E-mail: 0 400 800 1200 1600 [email protected] MED4 gene 1768 24 MARCH 2006 VOL 311 SCIENCE www.sciencemag.org REPORTS proteins; and a cyanophage-like homolog of entially expressed, including seven hli genes represented in the Sargasso Sea data set (Fig. phoH thought to be involved in the phosphate (table S1) that in Synechocystis encode proteins 2B, fig. S2). In MED4 and MIT9312, these stress response (15). ISL3 in this strain contains that accumulate when cells absorb excess ex- islands contain about half of the hli genes, a paralog of psbF, which encodes part of citation energy (e.g., under high light, nutri- lack the tRNA genes implicated in integration cytochrome b559, thought to protect against ent limitation, and low temperatures) (17). of mobile elements, and contain a smaller frac- photoinhibition (18). Islands also contain genes Thus, 26% of all MED4 island genes are dif- tion of noncyanobacterial genes than do the involved in nutrient assimilation, including a ferentially expressed under P starvation or other islands. This finding suggests that the cyanate transporter and lyase in MED4 and two high-light stress; only one of these is differ- genes in these islands have become fixed in transporters, for manganese/iron and amino entially expressed under both conditions (con- this wild population. acids, in MIT9312 (fig. S1). served hypothetical gene PMM1416), suggesting Examination of 36 large genome fragments In addition to genes involved in potentially that island genes contribute to specific stress (1.1 Mb total sequence; median size 34 kb) growth-limiting processes, islands also contain responses. (table S2) from the Hawaii Ocean Time-Series genes that could play a role in selective mortal- The genome variation within the eMIT9312 Station (22) further confirms that a stable core ity. ISL4 in both MED4 and MIT9312 encodes clade Esensu (7)^ was examined in wild pop- genome surrounds islands of variability, because proteins involved in cell surface modification, ulations of Prochlorococcus by aligning short most fragments showed remarkable conserva- including biosynthesis of lipopolysaccharide, a genome fragments from the Sargasso Sea (21), tion of gene content and order with respect to the common phage receptor (19) (fig. S1). Phages where this clade dominates (7), against the MED4 and MIT9312 genomes. Thirty-four of are important agents of mortality in the oceans MIT9312 genome (Fig. 2B). Nearly constant the 36 fragments were more similar to MIT9312 (20), and thus cell surface properties are likely coverage was observed, confirming a stable than to MED4; two contained rRNA operons, under strong selection. core genome, except for notable gaps at ISL1, confirming their phylogenetic affiliation with Clearly, for island genes to influence a cell_s ISL3, and ISL4.
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