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Biogeography of the Marine Actinomycete Salinispora Blackwell Publishing LtdOxford, UKEMIEnvironmental Microbiology1462-2912© 2006 The Authors; Journal compilation © 2006 Society for Applied Microbiology and Blackwell Publishing Ltd200681118811888Original ArticleSalin- ispora biogeographyP. R. Jensen and C. Mafnas Environmental Microbiology (2006) 8(11), 1881–1888 doi:10.1111/j.1462-2920.2006.01093.x Biogeography of the marine actinomycete Salinispora Paul R. Jensen* and Chrisy Mafnas and Staley, 2004), there is currently little empirical support Center for Marine Biotechnology and Biomedicine, for the ‘everything is everywhere but the environment Scripps Institution of Oceanography, University of selects’ paradigm (De Wit and Bouvier, 2006) when California, San Diego, CA, USA. applied at the species level. Without a better understand- ing of the extent to which geographical isolation affects the population structure of individual bacterial species, it Summary will not be possible to effectively estimate global species Marine actinomycetes belonging to the genus Salin- richness or to understand the forces driving speciation ispora were cultured from marine sediments collected among bacteria. at six geographically distinct locations. Detailed phy- Little emphasis has been given to the study of microbial logenetic analyses of both 16S rRNA and gyrB gene biogeography (Cho and Tiedje, 2000), and as a result it is sequences reveal that this genus is comprised of not clear if similar populations occupy analogous environ- three distinct but closely related clades correspond- ments on a global scale. The most outspoken support for ing to the species Salinispora tropica, Salinispora microbial cosmopolitanism comes from studies of microeu- arenicola and a third species for which the name karyotes (Findlay, 2002); however, this support is based ‘Salinispora pacifica’ is proposed. Salinispora areni- largely on the analysis of protozoan morphospecies. As cola was cultured from all locations sampled and pro- might be expected, evidence for cosmopolitanism among vides clear evidence for the cosmopolitan distribution environmental prokaryotes includes taxa with robust sur- of an individual bacterial species. The co-occurrence vival strategies, such as the spore-forming genus Bacillus, of S. arenicola with S. tropica and S. pacifica sug- for which it has been shown that migration rates are suf- gests that ecological differentiation as opposed to ficiently high to prevent geographical isolation (Roberts geographical isolation is driving speciation within the and Cohan, 1995). Additional evidence comes from a study genus. All Salinispora strains cultured to date share of fluorescent Pseudomonas strains where cosmopolitan- greater than 99% 16S rRNA gene sequence identity ism was evident by the analysis of 16S rDNA and, to a and thus comprise what has been described as a lesser extent, 16S-23S intergenic spacer regions (Cho and microdiverse ribotype cluster. The description of this Tiedje, 2000). Evidence for endemism was documented cluster as a new genus, containing multiple species, at the infraspecific level among the same Pseudomonas provides clear evidence that fine-scale 16S rDNA strains when higher resolution genomic fingerprinting sequence analysis can be used to delineate among methods were applied. Additional evidence for endemism closely related species and that more conservative is found among prokaryotes inhabiting extreme environ- operational taxonomic unit values may significantly ments where the barriers to surviving dispersal are high. underestimate global species diversity. This includes gas vacuolated sea ice bacteria (Staley and Gosink, 1999), the thermophilic archeon Sulfolobus (Whi- taker et al., 2003) and the thermophilic cyanobacterium Introduction Synecococcus (Papke et al., 2003). Bacterial biogeography remains an unresolved issue in Any discussion of species-level bacterial biogeography microbiology (Fenchel, 2003). Because of their small size, is affected by uncertainty surrounding the species concept high abundance and ease of dispersal, the prevailing for bacteria (Cohan, 2002; Gevers et al., 2005). Recently, hypothesis in the field is that free-living bacteria are it has been proposed that molecular sequence data can not subject to geographical isolation and, without this be used to define natural units of bacterial diversity that constraint, should exhibit a cosmopolitan distribution possess the fundamental properties of species (Cohan, (reviewed by Staley and Gosink, 1999; Martiny et al., 2002). These units can be recognized as clusters of 2006). While it is widely accepted that bacterial genera sequences that share greater similarity to each other than are widely distributed in their respective habitats (Hedlund to related sequences and are believed to delineate eco- logically distinct populations or ecotypes (Cohan, 2002). Ecotypes may arise through various processes (Gevers Received 21 November, 2005; accepted 4 March, 2006. *For corre- spondence. E-mail [email protected]; Tel. (+1) 858 534 7322; Fax et al., 2005) including geographical isolation or natural (+1) 858 558 3702. selection and can be difficult to resolve using highly con- © 2006 The Authors Journal compilation © 2006 Society for Applied Microbiology and Blackwell Publishing Ltd 1882 P. R. Jensen and C. Mafnas served loci such as the 16S rRNA gene (Fox et al., 1992; Actinoplanes auranticolor (ABO47491) 71 Catellatospora ferruginea (AF152108) Palys et al., 1997; Staley and Gosink, 1999). This has led Micromonospora olivasterospora (X92613) M. eburnea (AB107231) to an increased reliance on protein coding genes and, M. halophytica (X92601) more recently, multilocus sequence analysis for the reso- M. aurantiaca (X92604) M. rosaria (X92631) lution of intrageneric relationships (Gevers et al., 2005). M. endolithica (AJ560635) S. tropica (CNB-440) BA 89 (AY040617) In several cases, it has been demonstrated that named S. tropica (CNB-476) BA 89 S. tropica (CNB-392) BA 89 species are comprised of multiple ecotypes (Palys et al., S. tropica (CNB-536) BA 89 (AY040618) 2000), leading to the suggestion that the bacterial species 99 S. tropica (CNH-898) BA 00 (AY040622) S. tropica (CNR-699) BA 03 generally recognized today are in fact composites of mul- S. arenicola (CNS-205) PA 04 S. arenicola (CNS-051) PA 04 tiple ecotypes each possessing the dynamic properties of S. arenicola (CNB-458) BA 89 S. arenicola (CNB-527) BA 89 individual species (Cohan, 2002). S. arenicola (CNR-107) GU 02 (AY464534) We recently reported the discovery of the actinomycete S. arenicola (CNH-643) BA 99 (AY040619) S. arenicola (CNH-646) BA 99 (AY040620) genus Salinispora, which is widely distributed in tropical S. arenicola (CNH-877) BA 00 S. arenicola (CNH-905) BA 00 and subtropical marine sediments (Mincer et al., 2002; S. arenicola (CNQ-817) GU 02 56 S. arenicola (CNR-921) PA 04 Maldonado et al., 2005). To date, two species have been S. arenicola (CNQ-748) GU 02 S. arenicola (CNR-425) GU 02 (AY464533) formally described (S. arenicola and S. tropica), and a S. arenicola (CNQ-884) GU 02 third (‘S. pacifica’) is proposed based on DNA–DNA S. arenicola (CNQ-976) GU 02 S. arenicola (CNR-005) GU 02 hybridization. Salinispora belongs to the Micromonospo- S. arenicola (CNR-416) GU 02 S. arenicola (CNR-075) GU 02 raceae and is the first actinomycete genus known to S. arenicola (CNH-719 RS 00 S. arenicola (CNH-718) RS 00 require seawater for growth. As these bacteria produce S. arenicola (CNH-725) RS 00 (AY040621) resistant spores and have been cultured from worldwide S. arenicola (CNH-721) RS 00 S. arenicola (CNH-713) RS 00 100 locations, they represent model organisms to test hypoth- S. arenicola (CNP-161) USVI 01 100 S. arenicola (CNP-173) USVI 01 eses about bacterial biogeography and the processes that 100 S. arenicola (CNP-188) USVI 01 S. arenicola "A" (CNH-962 )SC 00 drive speciation. In this paper, the phylogenetic relation- S. arenicola "A" (CNH-963) SC 00 (DQ224162) ships of 152 strains were assessed using 16S rRNA and S. arenicola "A" (CNH-941) SC 01 (DQ224163) S. arenicola "A" (CNH-996) SC 01 gyrB gene sequences. The results provide compelling evi- S. arenicola "B" (CNP-152) SC 01 (DQ224164) S. arenicola "B" (CNP-193) SC 01 dence that an individual bacterial species comprised S. arenicola "B" (CNP-105) SC 00 S. arenicola "B" (CNH-964) SC 00 (AY040623) largely of 16S rDNA clones can have a cosmopolitan "S. pacifica" (CNH-732) RS 00 (DQ224165) distribution and that speciation within the genus Salin- "S. pacifica" (CNR-114) GU 02 (DQ224161) "S. pacifica" (CNQ-768) GU 02 ispora is not due to geographical isolation. "S. pacifica" (CNS-103) PA 04 (DQ224160) "S. pacifica" (CNS-143) PA 04 (DQ092624) 96 "S. pacifica" A (CNS-055) PA 04 (DQ224159) Blastococcus aggregatus (AJ430193) Results Propionibacterium propionicus 0.001 substitutions/site Salinispora strains were cultivated from all six tropical/ subtropical locations sampled. These locations included Fig. 1. Neighbour-joining phylogenetic tree created from 46 nearly complete (1449 nucleotides) 16S rRNA gene sequences from Salin- multiple collection sites within the Bahamas, where they ispora strains cultured from worldwide locations. The three major were originally discovered (Jensen et al., 1991), the US Salinispora phylotypes, consisting of the two formally described Virgin Islands, the Red Sea, the Sea of Cortez, Palau and species S. tropica and S. arenicola and the proposed species ‘S. pacifica’, are clearly delineated. Type strains representing the five Guam. In addition, strains were recently
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