The marine Roseobacter clade comprises several genera of marine bacteria related to the uncultured SAR83 cluster, the second most abundant marine picoplankton lineage. Cultivated representatives of this clade are physiologically heterogeneous, and only some have the capability for aerobic anoxygenic photosynthesis, a process of potentially great ecological importance in the world's oceans. In an attempt to correlate phylogeny with ecology, we investigated the diversity of Roseobacter clade strains from various marine habitats (water samples, biofilms, laminariae, diatoms, and dinoflagellate cultures) by using the 16S rRNA gene as a phylogenetic marker gene. The potential for aerobic anoxygenic photosynthesis was determined on the genetic level by PCR amplification and sequencing of the pufLM genes of the bacterial photosynthesis reaction center and on the physiological level by detection of bacteriochlorophyll (Bchl) a. A collection of ca. 1,000 marine isolates was screened for members of the marine Roseobacter clade by 16S rRNA gene-directed multiplex PCR and sequencing. The 42 Roseobacter clade isolates found tended to form habitat-specific subclusters. The pufLM genes were detected in two groups of strains from dinoflagellate cultures but in none of the other Roseobacter clade isolates. Strains within the first group (the DFL-12 cluster) also synthesized Bchl a. Strains within the second group (the DFL-35 cluster) formed a new species of Roseovarius and did not produce Bchl a under the conditions investigated here, thus demonstrating the importance of genetic methods for screening of cultivation-dependent metabolic traits. The pufL genes of the dinoflagellate isolates were phylogenetically closely related to pufL genes from Betaproteobacteria, confirming similar previous observations which have been interpreted as indications of gene transfer events.Phototrophy through bacteriochlorophyll (Bchl) a-mediated aerobic anoxygenic photosynthesis (40) has been estimated (based on in situ measurements of Bchl a) to be responsible for as much as 5 to 10% of the energy generation in the upper layers of the tropical oceans (12,18,19). The bacteria responsible for the process are thought to be related to the uncultivated marine SAR83 cluster within the alpha subclass of the Proteobacteria, which represents the second most abundant lineage of marine picoplankton bacteria after SAR11 (2,11,29). However, aerobic phototrophs have also been found in other genera of Alphaproteobacteria (Erythrobacter, Roseivivax, and Sphingomonas) and Betaproteobacteria (Roseateles) as well as among as yet uncultivated marine bacteria (2). In recent years, a large number of bacteria which are distantly related to the SAR83 cluster, and which form the Roseobacter clade, have been cultivated. Presently, 12 genera are recognized within this clade: Ketogulonicigenium,
Picoplankton bacteria from a North Sea water sample were cultured under a variety of different conditions (nutrients, temperature, light, agitation, adhesion). Fluorescent in situ hybridization (FISH) analysis of the enrichments showed complex communities which were dominated by gamma-Proteobacteria or beta-Proteobacteria, followed by alpha-Proteobacteria and bacteria from the Cytophaga/Flavobacterium/Bacteroides (CFB) cluster. Among 410 isolates, a high degree of diversity was found, both with respect to colony color and morphology and with respect to genetic diversity. Isolated bacteria were classified into the main taxa by a special PCR approach, termed signature PCR (SIG-PCR). It was based on an oligo primer mixture targeting 16S rDNA which yielded PCR products of taxon-specific lengths. Again, gamma-Proteobacteria dominated (48%), followed by alpha-Proteobacteria (20%). beta-Proteobacteria were rarely isolated (eight strains of 410). The CFB cluster comprised the second largest phylum (14%), and 7.5% of all isolates belonged to the high-GC Gram-positives. Thus, isolated bacteria were representative of enrichment communities with the exception of the beta-Proteobacteria, which were detected in high abundance in certain enrichments by FISH but not isolated, and the high-GC Gram-positives, which were cultivated but not detected by FISH. A genomic fingerprinting technique, randomly amplified polymorphic DNA, showed that among 58 CFB isolates only 18 identical genotypes were found, and among the 84 alpha-Proteobacteria only eight identical genotypes were present. The data show the enormous diversity of cultivated bacteria from picoplankton enrichment cultures of one North Sea water sample, which is only a small fraction of the total picoplankton community.
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