All bugs, big and small

The rapid progress in genome sequencing has launched a real revolution in microbiology and is beginning to impact other life sciences. Despite lingering debates on the principles for selection of organisms to be sequenced, the quality of data, and the astonishing number of uncharacterized proteins encoded in even simple bacterial genomes, no one can even imagine a return to the pregenomic ‘Dark Ages’. The ever-increasing flood of genomic data is now starting to include more and more environmentally relevant organisms. For a number of reasons, the first genome sequencing projects targeted mostly classical model organisms (Escherichia coli, Bacillus subtilis, yeast) and common bacterial pathogens (Haemophilus influenzae, mycoplasmas, chlamydiae, rickettsiae, streptococci and many others). Although the freshwater cyanobacterium Synechocystis sp. PCC6803 and the marine archaeon (archaebacterium) Methanococcus jannaschii were, respectively, the third and the fourth cellular organisms to have completely sequenced genomes, there has been relatively little effort to sequence environmental microorganisms. In the past couple of years this situation has changed dramatically. Every month now brings new complete genomes, at least some of which are relevant for environmental studies. These genomes are typically larger than those of pathogens and encode complex pathways for the utilization of diverse energy and carbon sources, biosynthesis of secondary metabolites, and environmental signal transduction. This is why, at the suggestion of the editors, Kenneth N. Timmis and David A. Stahl, we are starting this news feature that will provide an update on genomics projects relevant to environmental microbiology. Because it would be very hard to name a microorganism that is not relevant to environmental microbiology in one way or another, we would simply provide a list of the complete genome sequences that have appeared in public databases in the past two months and briefly describe what is unusual or otherwise interesting about them. The genomes finished in the 3-month period from December 2003 to February 2004 come in all shapes and forms and offer virtually unlimited opportunities for comparative studies (Table 1). The two largest ones, Photorhabdus luminescens and Rhodopseudomonas palustris, encode a huge variety of enzymes that allow them to prosper in diverse ecological niches. Rhodopseudomonas palustris, for example, can live as a photo- or chemoautotroph, using CO2 as a source of carbon, N2 as a nitrogen source and deriving energy from light or oxidation of inorganic electron donors, such as H2 or thiosulfate. It can also grow heterotrophically by degrading a variety of plant, animal, and human waste compounds, including lignin, heterocyclic aromatic compounds and even chlorinated benzoates. This metabolic versatility makes R. palustris and related purple photosynthetic bacteria an important component of the microbial community at the wastewater treatment plants. This ability to sustain a variety of lifestyles, however, requires R. palustris to carefully monitor the environmental parameters and tightly coordinate its metabolism, the task that is performed by a large network of signalling proteins. Rhodopseudomonas palustris encodes 67 sensory histidine kinases (including four of the recently described HWE type, Karniol and Vierstra, 2004), which is much more than is found in E. coli and Shewanella oneidensis that have similar genome sizes. Rhodopseudomonas palustris also encodes 31 methyl-accepting chemotaxis proteins and seven adenylate cyclases, at least five of which have sensory domains, 36 putative diguanylate cyclase (GGDEF) domains and 18 putative diguanylate phosphodiesterase (EAL) domains. Add to this almost 700 transport proteins and you’ll see why R. palustris is going to become a very convenient object for studying various aspects of environmental microbiology. The second genome in the list (Table 1) belongs to Photorhabdus luminescens, a relatively benign symbiont of the entomopathogenic nematode Heterorhabditis bacteriophora, which is used by this nematode as a weapon against insect larvae. Once the larva is killed, the partners share the spoils by digesting the larval carcass. The bacteria grow to the stationary phase while the nematodes develop and sexually reproduce. It has been suggested that P. luminescens provides the nematode with some additional nutrients, serving as its true symbiont. In any case, the main role of this bacterium is to serve as a weapon, and not a very smart one at that. Despite having a larger genome than R. palustris, P. luminescens encodes only 18 histidine kinases, two methyl-carrier proteins, and no adenylate cyclases, GGDEF or EAL domains. Well, a fighter does not need to be particularly sensitive; it just needs certain survival skills. And the latter ones – adhesins, toxins, other virulence factors – are plentiful in its genome. Photorhabdus luminescens even encodes several polyketide synthases and colicin-like proteins that should help it fend off potential bacterial competitors. All these systems deserve further studies that could also help us better understand the natural mechanisms of insect control. The greatest impact of the genomic sequence on understanding a previously obscure organism can be expected in case of Bdellovibrio bacteriovorus. This δ-proteobacterium infects many Gram-negative bacteria, settles in the periplasm of the host cell, and uses the host as a source of nutrients, gradually consuming the content of the host cell cytosol until there remains nothing to feed on. Bdellovibrio bacteriovorus attacks a wide range of hosts that includes a number of human, animal and plant pathogens. There is some evidence that it plays a key role in the natural purification of rivers, lakes and wastewater from contamination by (other) bacteria. Amazingly, the genome sequence shows that this fearsome predator is just a garden-variety proteobacterium with a typical set of proteolytic and saccharolytic enzymes. Several amino acid biosynthetic pathways are missing, reflecting adaptation of B. bacteriovorus to intracellular parasitism. Other biosynthetic pathways, however, are encoded in its genome, indicating the relatively low degree of parasitism-related gene loss. This is consistent with the relatively large (3.8 Mb) genome size of B. bacteriovorus, which is more typical for free-living bacteria than for obligate parasites. Genome analysis has already brought an important conclusion that, contrary to early beliefs, B. bacteriovorus does not incorporate host genes into its genome. Several hit (host interaction) genes have been identified, but the detailed mechanisms of bdellovibrial infection still remain to be studied. Like B. bacteriovorus, Geobacter sulfurreducens is a δ-proteobacterium but these two relatives with almost the same genome size couldn’t be more different. Geobacter is a free-living inhabitant of the underground environments, famous for its capability to use a wide variety of electron acceptors, including Fe3+, Co3+, elemental sulphur, fumarate, malate and many others. Its genome sequence produced sort of a shocker: the presumed obligate anaerobe was found to encode numerous catalases, peroxidases, superoxide dismutases, suggesting that it could survive in aerobic conditions. A detailed analysis of its genome in comparison with the forthcoming genome of Desulfovibrio vulgaris should yield important clues to the future use of Geobacter spp. in bioremediation.