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Unsuspected Diversity Among Marine Aerobic Anoxygenic Phototrophs

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Unsuspected Diversity Among Marine Aerobic Anoxygenic Phototrophs letters to nature 29. Houghton, R. A. & Hackler, J. L. Emissions of carbon from forestry and land-use change in tropical a BAC 56B12 Asia. Glob. Change Biol. 5, 481±492 (1999). BAC 60D04 30. Kauppi, P. E., Mielikainen, K. & Kuusela, K. Biomass and carbon budget of European forests, 1971 to 0.1 BAC 30G07 1990. Science 256, 70±74 (1992). 100 cDNA 0m13 cDNA 20m11 Supplementary Information accompanies the paper on Nature's website env20m1 (http://www.nature.com). 76 env20m5 cDNA 20m22 99 env0m2 Acknowledgements cDNA 20m8 R2A84* We thank B. Stephens for comments and suggestions on earlier versions of the manuscript. 72 R2A62* R2A163* This work was supported by the NSF, NOAA and the International Geosphere Biosphere 100 Program/Global Analysis, Interpretation, and Modeling Project. S.F. and J.S. were Rhodobacter capsulatus Rhodobacter sphaeroides α-3 supported by NOAA's Of®ce of Global Programs for the Carbon Modeling Consortium. Rhodovulum sulfidophilum* Correspondence and requests for materials should be addressed to A.S.D. 100 Roseobacter denitrificans* 73 Roseobacter litoralis* (e-mail: [email protected]). MBIC3951* 61 82 cDNA 0m1 100 cDNA 20m21 99 env0m1 envHOT1 100 Erythrobacter longus* Erythromicrobium ramosum ................................................................. 100 96 Erythrobacter litoralis* α-4 98 MBIC3019* Unsuspected diversity among marine Sphingomonas natatoria cDNA 0m20 aerobic anoxygenic phototrophs 96 Thiocystisge latinosa γ Allochromatium vinosum Rhodopseudomonas palustris Oded BeÂjaÁ*², Marcelino T. Suzuki*, John F. Heidelberg³, Rhodospirillum rubrum α–1 α William C. Nelson³, Christina M. Preston*, Tohru Hamada§², 56 Rhodomicrobium vannielii -2 Rhodocyclus tenuis 52 Jonathan A. Eisen³, Claire M. Fraser³ & Edward F. DeLong* Rubrivivax gelatinosus Roseateles depolymerans β * Monterey Bay Aquarium Research Institute, Moss Landing, Rhodoferax fermentans California 95039-0628, USA 100 envHOT2 100 envHOT3 ³ The Institute for Genomic Research, Rockville, Maryland 20850, USA cDNA 20m10 67 § Marine Biotechnology Institute, Kamaishi Laboratories, Kamaishi City, BAC 29C02 99 BAC 39B11 Iwate 026-0001, Japan 100 BAC 52B02 54 BAC 24D02 .............................................................................................................................................. BAC 65D09 Aerobic, anoxygenic, phototrophic bacteria containing bacterio- Chloroflexus aurantiacus chlorophyll a (Bchla) require oxygen for both growth and Bchla b synthesis1±6. Recent reports suggest that these bacteria are widely 100 Roseobacter denitrificans* 0.1 52 Roseobacter litoralis* distributed in marine plankton, and that they may account for up 91 to 5% of surface ocean photosynthetic electron transport7 and R2A84* 100 R2A62* 8 α-3 11% of the total microbial community . Known planktonic 100 MBIC3951* anoxygenic phototrophs belong to only a few restricted groups 95 Rhodobacter capsulatus within the Proteobacteria a-subclass. Here we report genomic Rhodobacter sphaeroides analyses of the photosynthetic gene content and operon organiza- Rhodovulum sulfidophilum* tion in naturally occurring marine bacteria. These photosynthetic 95 Erythromicrobium ramosum 82 Erythrobacter longus* gene clusters included some that most closely resembled those of 69 Erythrobacter litoralis* α-4 Proteobacteria from the b-subclass, which have never before been 100 MBIC3019* observed in marine environments. Furthermore, these photosyn- 61 Sphingomonas natatoria 65 thetic genes were broadly distributed in marine plankton, and Rhodomicrobium vannielii α-2 actively expressed in neritic bacterioplankton assemblages, indi- 98 Rhodopseudomonas palustris α cating that the newly identi®ed phototrophs were photosyntheti- 69 Rhodospirillum rubrum -1 cally competent. Our data demonstrate that planktonic bacterial 100 Rubrivivax gelatinosus 100 Roseateles depolymerans assemblages are not simply composed of one uniform, widespread β class of anoxygenic phototrophs, as previously proposed8; rather, 100 Rhodoferax fermentans Rhodocyclus tenuis these assemblages contain multiple, distantly related, photo- 100 100 Thiocystis gelatinosa γ synthetically active bacterial groups, including some unrelated Allochromatium vinosum to known and cultivated types. Chloroflexus aurantiacus Most of the genes required for the formation of bacteriochloro- phyll-containing photosystems in aerobic, anoxygenic, photo- Figure 1 Phylogenetic relationships of pufM gene (a) and rRNA (b) sequences of AAP trophic (AAP) bacteria are clustered in a contiguous, 45-kilobase bacteria. a, b, Evolutionary distances for the pufM genes (a) were determined from an (kb) chromosomal region (superoperon)6. These include bch and crt alignment of 600 nucleotide positions, and for rRNA genes (b) from an alignment of 860 genes coding for the enzymes of the bacteriochlorophyll and nucleotide sequence positions. Evolutionary relationships were determined by neighbour- carotenoid biosynthetic pathways, and the puf genes coding for joining analysis (see Methods). The green non-sulphur bacterium Chloro¯exus the subunits of the light-harvesting complex (pufB and pufA) and aurantiacus was used as an outgroup. pufM genes that were ampli®ed by PCR in this the reaction centre complex (pufL and pufM). To better describe the study are indicated by the env pre®x, with `m' indicating Monterey, and HOT indicating nature and diversity of planktonic, anoxygenic, photosynthetic Hawaii ocean time series. Cultivated aerobes are marked in light blue, bacteria cultured bacteria, we screened a surface-water bacterial arti®cial chromo- from sea water are marked with an asterisk, and environmental cDNAs are marked in red. Photosynthetic a-, b- and g-proteobacterial groups are indicated by the vertical bars to the right of the tree. Bootstrap values greater than 50% are indicated above the branches. ² Present addresses: Department of Biology, Technion-Israel Institute of Technology, Haifa 32000, Israel (O.B.); Nara Institute of Science and Technology, Takayama, Ikoma 630-0101, Japan (T.H.). The scale bar represents number of substitutions per site. 630 © 2002 Macmillan Magazines Ltd NATURE | VOL 415 | 7 FEBRUARY 2002 | www.nature.com letters to nature some (BAC) library9 prepared from surface-water marine bacterio- smaller fragment (156 nucleotides) of the pufM gene revealed ®ve plankton, for clones containing pufL and pufM10,11 genes. different groups of pufM in a Monterey Bay pufM cDNA gene library Several puf-containing BAC clones were identi®ed in screens (cDNAs in Fig. 1). One cDNA group clustered with the aerobic using primers10 designed to amplify almost the entire pufL and marine phototroph Roseobacter denitri®cans, another with strain pufM region (1520±1580 nucleotides). In addition, several coastal R2A84, and one was most similar to the pufM sequence from a g- a-proteobacterial strains previously isolated off the Oregon coast proteobacterium, Thiocystis gelatinosa.TwopufM cDNA groups were also screened (R2A strains)12. The pufM phylogenetic tree clustered with the different BAC clones, implying that these BAC (Fig. 1a) encompassed two principal clades, one containing a-3 and inserts originate from bacteria that were actively expressing photo- a-4 proteobacteria and one containing a-1, a-2, b- and g-proteo- synthetic genes. bacteria representatives, in agreement with an earlier study10. The To better characterize the bacteria from which these photosyn- BAC clones fell into three groups on the basis of pufM gene thetic operons originated, the BAC inserts (29C02, 41 kb; 60D04, phylogeny (Fig. 1a). One group (BAC clones 30G07, 56B12 and 103 kb; 65D09, 87 kb) were fully sequenced and the photosynthetic 60D04) was most closely related to pufM from a-proteobacteria operons compared with those of cultured proteobacteria. The isolates R2A62 and R2A84 (ref. 12) (Roseobacter-like, Fig. 1b), and operon organization of BAC clone 65D09 (and 29C02; data not was placed in the group containing a-3 Proteobacteria. The other shown), which falls inside the a-1/a-2/b/g pufM cluster, is con- two groups (29C02, 39B11 and 24D02, 52B02, 65D09) branched siderably different from the operon organization of any previously together, and were most similar to the freshwater b-proteobacter- reported photosynthetic organism (Fig. 2). Clones 65D09 and ium Rhodoferax fermentans (Fig. 1a, b). puf genes were also 29C02 are similar in their photosynthetic operon organization ampli®ed by polymerase chain reaction (PCR) from DNA extracts (data not shown), and when compared with both a-orb-proteo- of a mixed bacterioplankton assemblage, sampled at the same bacterial (Rhodobacter sphaeroides13 and Rubrivivax gelatinosus14, location as where the BAC library originated: Monterey Bay, respectively) operon organization, more closely resemble the b- California. These Monterey Bay pufM sequences clustered with proteobacterial operon (Fig. 2). BAC clone 60D04, which is related BAC clones 30G07, 56B12 and 60D04, the a-proteobacteria isolates to a-3 proteobacteria (on the basis of pufM sequences), also differs R2A62 and R2A84 (env0m2, env20m1 and env20m5), and the signi®cantly in gene arrangement from any other photosynthetic group composed of Roseobacter isolates (env0m1). The phyloge- operon organization reported to date. It most closely resembles the netic relationships of pufM genes were generally consistent with photosynthetic operons from Rhodobacter capsulatus8 and R. those determined from ribosomal RNA gene sequences, with the sphaeroides13,15, in both organization
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