Overview of light-mediated processes in biology. Organisms sense visible and UV light that they use for growth, adaptation, and defense/repair. Light sensing is carried out by antenna molecules with a photoactive pigment, such as carotenoids, phycocyanin, phycoerythrin, or rhodopsins. Photosynthetic bacteria can process the light energy through a reaction center and store it as ATP via a proton gradient. Bacteria living in high-light environments must also protect against and repair UV damage. Extracellular and intracellular UV-absorbing compounds such as scytonemin and mycosporine-like amino acids act as a natural sunscreen, while photolyase enzymes reverse point mutations in UV-damaged DNA by using a photon of blue light to catalyze the repair reaction. Finally, bacteria living in variable-light environments can adapt to the changing light conditions in a number of ways, e.g., by moving to a more favorable environment via phototaxis, reconfiguring the wavelength specificity of light-sensing antennae via adaptation proteins, or providing their own light via luminescence.

BLUF operons from genomes and metagenomes. BLUF domain proteins are shown in blue (center), with none containing additional domains. Genome neighbors include genes that function in phototaxis, nucleotide metabolism, repression of anoxygenic photosynthesis, and virulence, primarily from the Alphaproteobacteria (Rhodopseudomonas and Rhodobacter), Betaproteobacteria (Ralstonia and Chromobacterium), and Gammaproteobacteria (Shewanella and Psychrobacter). Novel metagenome neighbors include genes that function in luciferase synthesis, nitrate metabolism, and quorum sensing, primarily from Rhodopseudomonas and Comamonaceae.

Photolyase/cryptochrome subfamilies representing 1,196 sequences from sequenced genomes and four metagenomes. The tree recovers the known groupings of CPD-I and CPD-II photolyases and animal and DASH cryptochromes (plant cryptochromes, the fifth known group, are not shown here). In addition, we discovered two novel subfamilies of photolyases with 38 (family I) and 54 members (family II) that appear to originate from diverse members of the Alphaproteobacteria and Cyanobacteria.

Trends in the increase of genomic data and represented habitats. The number of sequenced ORFs continues to increase exponentially, accompanied by an increase in the number and complexity of represented habitats. In 1995, two sequenced organisms (Haemophilus influenzae and Mycoplasma pneumoniae) contributed just a few thousand genes to the public databases and represented a single habitat (organism associated). By 2008, well over 10 million genes from over 150 distinct habitats have been sequenced. Raw habitat and sequence data were collected from the Genomes Online database (43), and habitats were classified into the categories mentioned above using the Habitat-Lite terms of Environment Ontology (32). When an organism was reported to have multiple habitats, the primary one was used. “Extreme environment” corresponds to the Environment Ontology categories “hot spring,” “hydrothermal vent,” and “extreme environment.” “Sediment/sludge” corresponds to the Environment Ontology categories “sediment,” “sludge,” and “biofilm.” Note that (i) dates reported for each sequence are publication dates, even if the genome was released to the public earlier in database form, and (ii) the numbers for 2008 represent the available data until June 2008.

Abundances of light-sensing proteins in metagenomes. (A) Total number of proteins orthologous to 20 query proteins (columns) in 373 sequenced genomes (top row) and five metagenomes (remaining rows). (B) Number of proteins as a percentage of the total number of predicted proteins per environment. Rows labeled in gray are subsamples. Columns are labeled as follows (see Table 1 for details): psa, photosystem I subunits ABC; psb, photosystem II subunits ABDEHIJKLF; pet, photosynthetic electron transfer subunits A123; apc, allophycocyanin; cpc, phycocyanin; kaiAB, circadian clock regulators; bluf, blue-light flavin adenine dinucleotide-binding domain-containing proteins; slr0359/plpA, blue-light-absorbing phototropins; cph1 and cph2, red- and far-red-absorbing phytochromes; taxD1, photoreceptor for phototaxis; cry, DNA photolyase and cryptochrome families; carot, water-soluble carotenoids as intracellular UV sunscreen; scyto, scytonemin as extracellular sunscreen; taxP1, phototaxis putative regulatory element; taxY1, phototaxis CheY-like protein; taxAY1, phototaxis histidine kinase; rcaE, complementary chromatic adaptation protein. Growth and repair proteins are more abundant in high-light environments than invariable-light ones, whereas sensing and adaptation proteins are more abundant in variable-light environments than in high-light ones. In particular, photolyase DNA repair proteins are overrepresented in the high-UV environment of surface seawater compared to all other environments. BLUF domain blue-light-sensing proteins are extremely rare in both genomes and environments, although the majority are found in surface rather than deep water. The red-light sensors Cph1 and Cph2 are overrepresented in deep water rather than primarily blue surface water. RcaE chromatic adaptation proteins are overrepresented in variable-light environments, such as the deep sea and lower (darker) layers of the microbial mat.

RcaE domain variations in sequenced bacteria and plants. Whereas the majority of bacterial proteins have the conserved domain architecture of GAF-PAS-PAC-HisKA-HATPase-REC, many additional architectures with different signal transduction domains, multiple sensing domains, and multiple receiver domains exist.