Aerobic Anoxygenic Photosynthesis in Roseobacter Clade Bacteria from Diverse Marine Habitats

Abstract

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,

Expressed sequence tag profiles from calcifying and non-calcifying cultures of Emiliania huxleyi

“…f/50 plus peptone, yeast extract, casamino acids) after 14 to 21 days incubation when incubated in the light or the dark, and 16S rDNA analysis identified these cells as Erythrobacter/Roseobacter species. These marine, aerobic anoxygenic phototrophic bacteria can be isolated by enrichment under photoheterotrophic conditions but grow very poorly photoautotrophically (CO 2 as sole carbon source) (Allgaier et al 2003;Francis et al 2001). In addition, cultures of E. huxleyi CCMP 1516 used for library constructions were grown in f/2 or f/50 media supplemented with low levels of kanamycin (25 mg/ml), which inhibited growth of these prokaryotic contaminants.…”

Cluster Analysis as Selection and Dereplication Tool for the Identification of New Natural Compounds from Large Sample Sets

“…Most strains investigated were isolated from diverse habitats of the North Sea, including dinoflagellate cultures (strain designation DFL), picoplancton (Pic), water column samples (Hel), biofilm developed on glass plates (Bio), Laminaria surfaces (LM) and diatoms (DT). Details of the isolation procedure can be found in [15]. Strains were identified by sequencing the 16S rRNA gene as described in [15].…”

“…Details of the isolation procedure can be found in [15]. Strains were identified by sequencing the 16S rRNA gene as described in [15]. Seawater-based solns.…”

Diversity and abundance of aerobic anoxygenic phototrophic bacteria in two cyanobacterial bloom-forming lakes in China

“…Phylogenetic analysis based on pufM and other photosynthesis genes suggests that Alphaproteobacterial and Gammaproteobacterial AAP bacteria are abundant in oceans and saline lakes, whereas Betaproteobacteria are predominant in freshwater bodies (Yurkova et al, 2002;Allgaier et al, 2003;Karr et al, 2003;Waidner and Kirchman, 2005Jiang et al, 2009). The discovery of AAP bacteria in open seas suggests that AAP bacteria can adapt to oligotrophic waters because light might provide supplementary energy in low-nutrient conditions (Kolber et al, 2000(Kolber et al, , 2001.…”