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Halobacteria

(3)

Aerobic chemoorganoheterotroph

Purple membrane; bacteriorhodopsin

Bacteriorhodopsin

aThe numbers of photosynthetic species described for each taxon are given in parenthesis.

BChl = bacteriochlorophyll, car = carotenoids, Chl = chlorophyll, cls = chlorosomes, icm = intracellular membranes, PBS = phycobilisomes, thy = thylacoids.

aThe numbers of photosynthetic species described for each taxon are given in parenthesis.

BChl = bacteriochlorophyll, car = carotenoids, Chl = chlorophyll, cls = chlorosomes, icm = intracellular membranes, PBS = phycobilisomes, thy = thylacoids.

most types contain phycobiliproteins as light-harvesting pigments. These multimeric proteina-ceous structures are found on the cytoplasmic face of the intracellular thylakoid membranes and contain phycobilins as light-harvesting pigments. All Cyanobacteria are able to grow using CO2 as the sole sou rce of carbon, which they fix using primarily the reductive pentose phosphate pathway (see Carbon Metabolism of Phototrophic Prokaryotes in this Chapter). Their chemoorganotrophic potential typically is restricted to the mobilization of reserve polymers (mainly starch but also polyhydroxyal-kanoates) during dark periods, although some strains are known to grow chemoorganotrophi-cally in the dark at the expense of external sugars. Owing to their ecological role, in many cases indistinguishable from that of eukaryotic microalgae, the cyanobacteria had been studied originally by botanists. The epithets "blue-green algae," "Cyanophyceae," "Cyanophyta," "Myxo-phyceae," and "Schizophyceae" all apply to the cyanobacteria. Two main taxonomic treatments of the Cyanobacteria exist, and are widely used, which divide them into major groups (orders) on the basis of morphological and life-history traits. The botanical system (Geitler, 1932 recognized 3 orders, 145 genera and some 1300 spe cies, but it has recently been modernized (Anagnostidis and Komarek, 1989, Komarek and Anagnostidis, 1989). The bacteriological system (Stanier, 1977; Rippka et al., 1979; Castenholz, 1989), relies on the study of cultured axenic strains. It recognizes five larger groups or orders, separated on the basis of morphological characters. Genetic (i.e., mol% GC, DNA-DNA hybridization) as well as physiological traits have been used to separate genera in problematic cases.

Previously, a separate group of organisms with equal rank to the cyanobacteria, the so-called "Prochlorophytes" (with two genera, Prochlo-ron, a unicellular symbiont of marine invertebrates, and Prochlorothrix, a free-living filamentous form) had been recognized (Lewin, 1981). They were differentiated from cyanobacteria by their lack of phycobiliproteins (Fig. 2) and the presence of chlorophyll b. The recently recognized genus Prochlorococcus of marine picoplankters could be included here, even though the major chlorophylls in this genus are divinyl-Chl a and divinyl-Chl b. Fourteen Prochloron isolates from different localities and hosts have been found to belong to a single species by DNA-DNA hybridization studies (Stam et al., 1985; Holtin et al., 1990). Some of the original distinctions leading to the separation of the Chl b-containing oxyphotobacteria from the cyanobacteria are questionable, since at least in one strain of Prochloroccoccus marinus, functional phycoerythrin (Lokstein et al., 1999), and genes encoding for phycobiliproteins have been detected (Lokstein et al., 1999). Additionally, phylogenetic analysis of 16S rRNA genes indicate that the three genera of Chl b-containing prokaryotes arose independently from each other and from the main plastid line (see Evolutionary Considerations in this Chapter), a result that is supported by the comparative sequence analysis of the respective Chl a/b binding proteins (Laroche et al., 1996; Vanders taay et al., 1998). Thus "Prochlorophytes" are just greenish cyanobacteria, and are not treated separately here. The recent discovery of Chl d-containing symbionts in ascidians (Acaryochloris marina, Miyashita et al., 1996) once again demonstrates the evolutionary diversification of light-harvesting capabilities among oxyphotobacteria (see Competition for Light in this Chapter). While the phylogenetic affiliation of Acaryochloris marina has not been presented as yet, ultrastructural and chemotaxonomic characters predict that A. marina belongs to the cyanobacterial radiation as well.

According to phylogenetic analysis of 16S rRNA sequences, the Cyanobacteria are a diverse phylum of organisms within the bacterial radiation, well separated from their closest relatives (Giovanonni, 1988; Wilmotte, 1995; Turner, 1887; Garcia-Pichel, 1999; Fig. 1). These analyses support clearly the endosymbiotic theory for the origin of plant chloroplasts, as they place plastids (from all eukaryotic algae and higher plants investigated) in a diverse, but monophyletic, deep-branching cluster (Nelissen et al., 1995). Phylogenetic reconstructions show that the present taxonomic treatments of the cyanobac-teria diverge considerably from a natural system that reflects their evolutionary relationships. For example, separation of the orders Chroococcales and Oscillatoriales (Nelissen et al., 1995; Reeves, 1996), and perhaps also the Pleurocapsales (Turner, 1887; Garcia-Pichel et al., 1998) is not supported by phylogenetic analysis. The hetero-cystous cyanobacteria (comprising the two orders Nostocales and Stigonematales) form together a monophyletic group, with relatively low sequence divergence, as low as that presented by the single accepted genus Spirulina (Nübel, 1999). A grouping not corresponding to any official genus, the Halothece cluster, gathers unicellular strains of diverse morphology that are extremely tolerant to high salt and stem from hypersaline environments (Garcia-Pichel et al., 1998). A second grouping, bringing together very small unicellular ope n-ocean cyanobacteria (picoplankton) includes only marine picoplank-tonic members of the genera Synechococcus and all Prochlorococcus. Several other statistically well-supported groups of strains that may or may not correspond to presently defined taxa can be distinguished. The botanical genus "Microcystis" of unicellular colonial freshwater plankton species is very well supported by phylogenetic reconstruction, as is the genus Trichodesmium of filamentous, nonheterocystous nitrogen-fixing species typical from oligotrophic marine plankton of the tropics. The picture that emerges from these studies is that sufficient knowledge of ecological and physiological characteristics can lead to a taxonomic system that is largely congruent to the 16S rRNA phylogeny.

A different principle of conversion of light energy into chemical energy is found in the Halo-bacteria. These archaea are largely confined to surface layers of hypersaline aquatic environments and grow predominantly by chemoorga-noheterotrophy with amino or organic acids as electron donors and carbon substrates, generating ATP by respiration of molecular oxygen. In the absence of oxygen, several members are capable of fermentation or nitrate respiration. At limiting concentrations of oxygen, at least three of the described species of Halobacteria (Halobacterium halobium, H. salinarium, H. sod-omense) synthesize bacteriorhodopsin (Oester-helt and Stoeckenius, 1973), a chromoprotein containing a covalently bound retinal. Bacterior-hodopsin is incorporated in discrete patches in the cytoplasmic membrane ("purple membrane"). However, these prokaryotes have only a very limite d capability of light-dependent growth. Only slow growth and one to two cell doublings could be demonstrated experimentally (Hartmann et al., 1980; Oesterhelt and Krippahl, 1983). The fact that rhodopsin-based photosynthesis has been found only in the phylogeneti-cally tight group of Halobacteria may indicate that, because of its lower efficiency, this type of light utilization is of selective advantage only under specific (and extreme) environmental conditions. Further information on the biochemistry, physiology and ecology of this group may be found in the chapters, Introduction to the Classification of Archaea and The Family Halo-bacteriaceae.

During the past years, culture-independent 16S rDNA-based methods have been used for the investigation of the composition of natural communities of phototrophic prokaryotes. These studies have provided evidence that more than one genotype of Chloroflexus occur in one hot spring microbial mat and that four previously unkown sequences of cyanobacteria dominate in the same environment (Ferris et al., 1996; Ruff-Roberts et al., 1994; Weller et al., 1992). Similarly, nine different partial 16S rDNA sequences of Chromatiaceae and green sulfur bacteria, which differed from all sequences previously known, were retrieved from two lakes and one intertidal marine sediment (Coolen and Overmann, 1998; Overmann et al., 1999a).

However, 16S RNA signatures from natural populations were indistinguishable from those of cultured strains in the case of cyanobacteria with conspicuous morphologies, such as the cosmopolitan Microcoleus chthonoplastes (Garcia-Pichel et al., 1996) from intertidal and hypersaline microbial mats or Microcoleus vaginatus from desert soils (F. Garcia-Pichel, C. López-Cortés and U. Nübel, unpublished observations). In a similar manner, the 16S rRNA sequence of an isolated strain of Amoebobacter purpureus (Chromatiaceae) was found to be identical to the environmental sequence dominating in the chemocline of a meromictic salt lake (Coolen and Overmann, 1998; Overmann et al., 1999a). Obviously, the limited number of isolated and characterized bacterial strains rather than an alleged "nonculturability," at least in some cases, accounts for our inability to assign ecophysiolog-ical properties to certain 16S rRNA sequence types. This point is illustrated for extremely hal-otolerant unicellular cyanobacteria by the fact that only after a physiologically coherent group of strains was defined on the basis of newly characterized isolates (Garcia-Pichel et al., 1998) could the molecular signatures retrieved from field samples be assigned correctly.

It has to be concluded that 1) the numbers of species listed in Table 1 do not reflect the full phylogenetic breadth at least in the four groups of anoxygenic phototrophic prokaryotes as well as in morphologically simple Cyanobacteria, and 2) that the physiology and ecology of those species of phototrophic prokaryotes that are dominant in the natural environment in some cases may differ considerably from known type strains.

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