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At least 19 recordsLinked to original sources
PubMed2006

Prokaryotic photosynthesis and phototrophy illuminated.

Genome sequencing projects are revealing new information about the distribution and evolution of photosynthesis and phototrophy. Although coverage of the five phyla containing photosynthetic prokaryotes (Chlorobi, Chloroflexi, Cyanobacteria, Proteobacteria and Firmicutes) is limited and uneven, genome sequences are (or soon will be) available for >100 strains from these phyla. Present knowledge of photosynthesis is almost exclusively based on data derived from cultivated species but metagenomic studies can reveal new organisms with novel combinations of photosynthetic and phototrophic components that have not yet been described. Metagenomics has already shown how the relatively simple phototrophy based upon rhodopsins has spread laterally throughout Archaea, Bacteria and eukaryotes. In this review, we present examples that reflect recent advances in phototroph biology as a result of insights from genome and metagenome sequencing.

Chlorobi↗
PubMed2004

A genomic timescale of prokaryote evolution: insights into the origin of methanogenesis, phototrophy, and the colonization of land.

BACKGROUND: The timescale of prokaryote evolution has been difficult to reconstruct because of a limited fossil record and complexities associated with molecular clocks and deep divergences. However, the relatively large number of genome sequences currently available has provided a better opportunity to control for potential biases such as horizontal gene transfer and rate differences among lineages. We assembled a data set of sequences from 32 proteins (approximately 7600 amino acids) common to 72 species and estimated phylogenetic relationships and divergence times with a local clock method. RESULTS: Our phylogenetic results support most of the currently recognized higher-level groupings of prokaryotes. Of particular interest is a well-supported group of three major lineages of eubacteria (Actinobacteria, Deinococcus, and Cyanobacteria) that we call Terrabacteria and associate with an early colonization of land. Divergence time estimates for the major groups of eubacteria are between 2.5-3.2 billion years ago (Ga) while those for archaebacteria are mostly between 3.1-4.1 Ga. The time estimates suggest a Hadean origin of life (prior to 4.1 Ga), an early origin of methanogenesis (3.8-4.1 Ga), an origin of anaerobic methanotrophy after 3.1 Ga, an origin of phototrophy prior to 3.2 Ga, an early colonization of land 2.8-3.1 Ga, and an origin of aerobic methanotrophy 2.5-2.8 Ga. CONCLUSIONS: Our early time estimates for methanogenesis support the consideration of methane, in addition to carbon dioxide, as a greenhouse gas responsible for the early warming of the Earths' surface. Our divergence times for the origin of anaerobic methanotrophy are compatible with highly depleted carbon isotopic values found in rocks dated 2.8-2.6 Ga. An early origin of phototrophy is consistent with the earliest bacterial mats and structures identified as stromatolites, but a 2.6 Ga origin of cyanobacteria suggests that those Archean structures, if biologically produced, were made by anoxygenic photosynthesizers. The resistance to desiccation of Terrabacteria and their elaboration of photoprotective compounds suggests that the common ancestor of this group inhabited land. If true, then oxygenic photosynthesis may owe its origin to terrestrial adaptations.

Bacteria↗
PubMed2001

Proteorhodopsin phototrophy in the ocean.

Proteorhodopsin, a retinal-containing integral membrane protein that functions as a light-driven proton pump, was discovered in the genome of an uncultivated marine bacterium; however, the prevalence, expression and genetic variability of this protein in native marine microbial populations remain unknown. Here we report that photoactive proteorhodopsin is present in oceanic surface waters. We also provide evidence of an extensive family of globally distributed proteorhodopsin variants. The protein pigments comprising this rhodopsin family seem to be spectrally tuned to different habitats--absorbing light at different wavelengths in accordance with light available in the environment. Together, our data suggest that proteorhodopsin-based phototrophy is a globally significant oceanic microbial process.

Amino Acid Sequence↗
PubMed1996

Anoxygenic phototrophy across the phylogenetic spectrum: current understanding and future perspectives

The phylogenetic heterogeneity of anoxygenic phototrophic bacteria has been revealed by 16S rRNA sequence analysis, the results of which have led to extensive taxonomic rearrangements within previously defined taxa of phototrophs and stimulated interest in this group of organisms. Anoxygenic photosynthetic bacteria can be found within 4 of the 12 phylogenetic lineages, and in some cases are highly related to non-photosynthetic members of these groups. The largest number of phototrophs are found in the class Proteobacteria. Comparative phylogenetic analysis using 23S rDNA sequences generally supports the topology obtained from 16S rDNA sequences. The photosynthetic reaction centers are conserved in all photosynthetic bacteria, and are of two types. One is shared by the Proteobacteria and Chloroflexus aurantiacus and is similar to Photosystem II of cyanobacteria, while heliobacteria and Chlorobium and relatives possess a reaction center similar to the cyanobacterial Photosystem I. These similarities are supported by sequence analysis of core reaction center peptides, but contradict phylogenies reconstructed from rRNA sequence analysis. Genome analysis by means of physical mapping has been performed for only three species of anoxygenic phototrophs. Some conservation of operon structure and gene sequence has been found within the Proteobacteria, but does not extend to other phototrophs.

Journal Article↗
PubMed2005

Community-level analysis of phototrophy: psbA Gene Diversity.

Photosynthetic organisms play a crucial role in the marine environment. In vast areas of the oceans, most of this marine production is performed by cells smaller than 2-3 microm (picoplankton). This chapter describes molecular analyses of the conserved photosynthetic psbA gene (protein D1 of photosystem II reaction center) as a diversity indicator of naturally occurring marine oxygenic picophytoplankton and of marine cyanophages carrying photosynthesis genes.

Chromosomes, Artificial, Bacterial↗
PubMed1976

Enzyme levels in relation to obligate phototrophy in chlamydobotrys.

During the transition from photoheterotrophic growth on acetate to phototrophic growth on carbon dioxide, there is a decrease in isocitrate lyase and increase in ribulose-1,5-diphosphate carboxylase activity in Chlamydobotrys stellata cultures. The increase in ribulose-1,5-diphosphate carboxylase activity is the result of protein synthesis, there being a close correlation between increase in enzyme activity and protein precipitated by antibody to ribulose-1,5-diphosphate carboxylase. The purified ribulose-1,5-diphosphate carboxylase was similar to the constitutive enzyme from other green algae having a molecular weight of 530,000 and composed of two types of subunit of molecular weight 53,000 and 14,000.Enzyme assays demonstrated an incomplete tricarboxylic acid cycle in cells growing photoheterotrophically on acetate or phototrophically on carbon dioxide. Although these cells lack alpha-ketoglutarate dehydrogenase and succinate thiokinase, a cyclic flow of acetate carbon is possible in the presence of the glyoxylate cycle enzymes but the yield of adenosine triphosphate from acetate oxidation may be insufficient to support heterotrophic growth, so rendering Chlamydobotrys an obligate phototroph.

Journal Article↗
PubMed1992

IRE1 encodes a putative protein kinase containing a membrane-spanning domain and is required for inositol phototrophy in Saccharomyces cerevisiae.

A novel gene, IRE1, of Saccharomyces cerevisiae was cloned through genetic complementation of a myoinositol auxotrophic mutant. The predicted amino acid sequence indicated that IRE1 encodes a protein of 126983 Da with two highly hydrophobic regions, probably a signal sequence and a membrane-spanning region. The carboxy-terminal region of IRE1 showed close sequence similarity to the catalytic domains of protein kinases. Disruption of the IRE1 locus caused myo-inositol auxotrophy. The IRE1 product is very likely a protein kinase required for myo-inositol synthesis.

Amino Acid Sequence↗
PubMed1998

Obligate phototrophy in cyanobacteria: more than a lack of sugar transport.

DNA hybridization using the Synechocystis PCC6803 glucose transporter gene, glcP, revealed a single homologous region in two facultative photoautotrophic strains out of three tested, and none in three obligate autotrophs. In one of the latter, Synechococcus PCC7942, integration of glcP into the chromosome resulted in glucose sensitivity. A subclone isolated as glucose-tolerant had lost glcP. Integration in a replicative vector allowed glucose transport and photoheterotrophic growth, but could not be maintained. Thus lack of sugar transport could explain cyanobacterial obligate autotrophy. However, at least in Synechococcus PCC7942, acquisition of such a transport capacity created a metabolic disequilibrium barely compatible with survival.

Bacteria↗
PubMed2000

Bacterial rhodopsin: evidence for a new type of phototrophy in the sea.

Extremely halophilic archaea contain retinal-binding integral membrane proteins called bacteriorhodopsins that function as light-driven proton pumps. So far, bacteriorhodopsins capable of generating a chemiosmotic membrane potential in response to light have been demonstrated only in halophilic archaea. We describe here a type of rhodopsin derived from bacteria that was discovered through genomic analyses of naturally occuring marine bacterioplankton. The bacterial rhodopsin was encoded in the genome of an uncultivated gamma-proteobacterium and shared highest amino acid sequence similarity with archaeal rhodopsins. The protein was functionally expressed in Escherichia coli and bound retinal to form an active, light-driven proton pump. The new rhodopsin exhibited a photochemical reaction cycle with intermediates and kinetics characteristic of archaeal proton-pumping rhodopsins. Our results demonstrate that archaeal-like rhodopsins are broadly distributed among different taxa, including members of the domain Bacteria. Our data also indicate that a previously unsuspected mode of bacterially mediated light-driven energy generation may commonly occur in oceanic surface waters worldwide.

Aerobiosis↗
PubMed2002

Coordinate regulation of energy transduction modules in Halobacterium sp. analyzed by a global systems approach.

The extremely halophilic archaeon Halobacterium NRC-1 can switch from aerobic energy production (energy from organic compounds) to anaerobic phototrophy (energy from light) by induction of purple membrane biogenesis. The purple membrane is made up of multiple copies of a 1:1 complex of bacterioopsin (Bop) and retinal called bacteriorhodopsin that functions as a light-driven proton pump. A light- and redox-sensing transcription regulator, Bat, regulates critical genes encoding the biogenesis of the purple membrane. To better understand the regulatory network underlying this physiological state, we report a systems approach using global mRNA and protein analyses of four strains of Halobacterium sp.: the wild-type, NRC-1; and three genetically perturbed strains: S9 (bat+), a purple membrane overproducer, and two purple membrane deficient strains, SD23 (a bop knockout) and SD20 (a bat knockout). The integrated DNA microarray and proteomic data reveal the coordinated coregulation of several interconnected biochemical pathways for phototrophy: isoprenoid synthesis, carotenoid synthesis, and bacteriorhodopsin assembly. In phototrophy, the second major biomodule for ATP production, arginine fermentation, is repressed. The primary systems level insight provided by this study is that two major energy production pathways in Halobacterium sp., phototrophy and arginine fermentation, are inversely regulated, presumably to achieve a balance in ATP production under anaerobic conditions.

Adenosine Triphosphate↗
PubMed2026

Phototrophicity and genomic composition in plant-associated Sphingomonas faeni strains.

Solar radiation impacts most life forms on Earth as an energy source or a regulatory signal. Still, relatively little is known about phototrophic potential and strategies of environmental bacteria beyond cyanobacteria. This study explores the phototrophy related genomic diversity of Sphingomonas faeni strains from boreal, sub-arctic and arctic regions. We analyzed the genomes of 25 plant-associated S. faeni strains isolated from Vaccinium myrtillus, Oxyria digyna, V. vitis-idaea, and Bistorta vivipara, along with a reference S. faeni genome MA-Olki. The strains showed diversity both in overall genome level but also in phototrophic capabilities: Seven strains were identified as aerobic anoxygenic phototrophic bacteria with a complete photosynthesis gene cluster, 16 strains contained xanthorhodopsin genes, and three strains were non-phototrophic, possessing no aerobic anoxygenic phototrophic or xanthorhodopsin genes. Aerobic anoxygenic phototrophic strains were found exclusively in Vaccinium hosts. O. digyna contained only xanthorhodopsin containing strains and B. vivipara showed xanthorhodopsin genes and one non-phototrophic strain. V. vitis-idaea hosted strains for all three different phototrophy categories. Phylogenetic analyses showed aerobic anoxygenic phototrophic positive strains forming a tight phylogenetic group. Xanthorhodopsin strains and non-phototrophic strains clustered into three different subgroups. Phototrophic strains had more photoreceptors. Aerobic anoxygenic phototrophic strains encoded two 5-aminolevulinic acid synthase isoenzymes, one from a hemT-like gene within the photosynthesis gene cluster and one from a hemA-like gene elsewhere in the genome. Our genomic analysis reveals substantial diversity in phototrophic potential among strains of a single bacterial species isolated from different host plants, possibly reflecting the distinct environmental cues each strain encountered.

aerobic anoxygenic phototrophy↗
PubMed2003

Mixotrophs combine resource use to outcompete specialists: implications for aquatic food webs.

The majority of organisms can be grouped into those relying solely on photosynthesis (phototrophy) or those relying solely on the assimilation of organic substances (heterotrophy) to meet their requirements for energy and carbon. However, a special life history trait exists in which organisms combine both phototrophy and heterotrophy. Such "mixotrophy" is a widespread phenomenon in aquatic habitats and is observed in many protozoan and metazoan organisms. The strategy requires investment in both photosynthetic and heterotrophic cellular apparatus, and the benefits must outweigh these costs. In accordance with mechanistic resource competition theory, laboratory experiments revealed that pigmented mixotrophs combined light, mineral nutrients, and prey as substitutable resources. Thereby, they reduced prey abundance below the critical food concentration of competing specialist grazers [Rothhaupt, K. O. (1996) Ecology 77, 716-724]. Here, we demonstrate the important consequences of this strategy for an aquatic community. In the illuminated surface strata of a lake, mixotrophs reduced prey abundance steeply. The data suggest that, as a consequence, grazers from higher trophic levels, consuming both the mixotrophs and their prey, could not persist. Thus, the mixotrophs escaped from competition with and losses to higher grazers. Furthermore, the mixotrophs structured prey abundance along the vertical light gradient, creating low densities near the surface and a pronounced maximum of their algal prey at depth. Such deep algal accumulations are typical features of nutrient-poor aquatic habitats, previously explained by resource availability. We hypothesize instead that the mixotrophic grazing strategy is responsible for deep algal accumulations in many aquatic environments.

Animals↗
PubMed1976

The capacity of phototrophic sulfur bacterium Thiocapsa roseopersicina for chemosynthesis.

Purple sulfur bacterium Thiocapsa roseopersicina strain BBS requiring vitamin B12 may grow in the dark in media containing no other organic compounds. Under such conditions the cells oxidize sulfide and thiosulfate with the use of O2 and assimilate carbon dioxide. After 10--30s assimilation of NaH14CO3 about 60% of radioactivity is found in phosphorylated compounds characteristic for the reductive pentose phosphate cycle. The possibility of the function of this cycle in the dark in the presence of O2 is confirmed by the capacity of cells grown under such conditions to synthesize ribulose-1,5-diphosphate carboxylase. All this evidence suggests the ability of T. roseopersicina to change from phototrophy to aerobic chemolithoautotrophy.

Aerobiosis↗
PubMed2005

Phylogenetic analyses of the core antenna domain: investigating the origin of photosystem I.

Phototrophy, the conversion of light to biochemical energy, occurs throughout the Bacteria and plants, however, debate continues over how different phototrophic mechanisms and the bacteria that contain them are related. There are two types of phototrophic mechanisms in the Bacteria: reaction center type 1 (RC1) has core and core antenna domains that are parts of a single polypeptide, whereas reaction center type 2 (RC2) is composed of short core proteins without antenna domains. In cyanobacteria, RC2 is associated with separate core antenna proteins that are homologous to the core antenna domains of RC1. We reconstructed evolutionary relationships among phototrophic mechanisms based on a phylogeny of core antenna domains/proteins. Core antenna domains of 46 polypeptides were aligned, including the RC1 core proteins of heliobacteria, green sulfur bacteria, and photosystem I (PSI) of cyanobacteria and plastids, plus core antenna proteins of photosystem II (PSII) from cyanobacteria and plastids. Maximum likelihood, parsimony, and neighbor joining methods all supported a single phylogeny in which PSII core antenna proteins (PsbC, PsbB) arose within the cyanobacteria from duplications of the RC1-associated core antenna domains and accessory antenna proteins (IsiA, PcbA, PcbC) arose from duplications of PsbB. The data indicate an evolutionary history of RC1 in which an initially homodimeric reaction center was vertically transmitted to green sulfur bacteria, heliobacteria, and an ancestor of cyanobacteria. A heterodimeric RC1 (=PSI) then arose within the cyanobacterial lineage. In this scenario, the current diversity of core antenna domains/proteins is explained without a need to invoke horizontal transfer.

Amino Acid Sequence↗
PubMed2000

Shifting roles of heterotrophy and autotrophy in coral energetics under varying turbidity.

Suspended particulate matter (SPM) strongly alters the trophic environment of photosymbiotic aquatic organisms. At high particles loads, phototrophic energy gains can be diminished due to light absorption by suspended particles, and stress from particle abrasion or deposition on tissues. However, energy gains are enhanced if organisms are able to use SPM as a food source. For photosymbiotic benthic suspension feeders, increases in SPM concentrations may require both phototrophic and heterotrophic acclimation to sustain a positive energy balance. This study provides an experimental analysis of the effects of contrasting light and SPM regimes on the energy budget (scope for growth) of two zooxanthellate corals (Goniastrea retiformis and Porites cylindrica). Using a factorial design in a flow-through tank system, corals were exposed for 2 months to shaded and unshaded conditions (equivalent to 3-4 m depth at 4 and 16 mg dry weight SPM l(-1), respectively) and a range of controlled SPM loads with a natural organic content ( approximately 3% w/w). In G. retiformis, rates of particle ingestion were a linear function of SPM concentration within a broad range (1-30 mg dry weight l(-1)). After 2 months of shading, photosynthetic acclimation was significant in G. retiformis, but did not compensate for the reduced light level, as daily respiration exceeded daily photosynthesis. However, in response to the prolonged shading, G. retiformis more than doubled its rate of particle feeding. At high SPM treatments (16 mg dw l(-1)), sediment feeding by this species compensated fully for the 35-47% lower phototrophy in the shaded treatment. Due to both photo- and heterotrophic plasticity, G. retiformis gained tissue and skeletal mass at all experimental levels of light and SPM. In contrast, rates of particle intake by P. cylindrica contributed <10% to the energy budget in shaded and <3% in unshaded conditions. Feeding rates of P. cylindrica were half-saturated at approximately 3 mg dry weight l(-1), and four- to eight-fold lower than those of G. retiformis. Skeletal growth was sustained, but tissue mass and lipid contents declined in shaded and high-SPM treatments, and carbon loss due to shading by SPM was not compensated for by particle feeding. Thus, due to a lack of photo- and heterotrophic plasticity, periods of high turbidity resulted in energy deficiency in P. cylindrica, and high turbidity conditions appeared physiologically unsustainable for this species. This study is the first to show heterotrophic plasticity in a symbiotic coral, and to show that such plasticity can offset stress from high particle loads. It demonstrates that changes in the trophic mode of some coral species are a mechanism for sustaining a positive energy balance in turbid environments, thereby broadening their physiological niche.

Journal Article↗
PubMed1999

2-Methylhopanoids as biomarkers for cyanobacterial oxygenic photosynthesis.

Oxygenic photosynthesis is widely accepted as the most important bioenergetic process happening in Earth's surface environment. It is thought to have evolved within the cyanobacterial lineage, but it has been difficult to determine when it began. Evidence based on the occurrence and appearance of stromatolites and microfossils indicates that phototrophy occurred as long ago as 3,465 Myr although no definite physiological inferences can be made from these objects. Carbon isotopes and other geological phenomena provide clues but are also equivocal. Biomarkers are potentially useful because the three domains of extant life-Bacteria, Archaea and Eukarya-have signature membrane lipids with recalcitrant carbon skeletons. These lipids turn into hydrocarbons in sediments and can be found wherever the record is sufficiently well preserved. Here we show that 2-methyl-bacteriohopanepolyols occur in a high proportion of cultured cyanobacteria and cyanobacterial mats. Their 2-methylhopane hydrocarbon derivatives are abundant in organic-rich sediments as old as 2,500 Myr. These biomarkers may help constrain the age of the oldest cyanobacteria and the advent of oxygenic photosynthesis. They could also be used to quantify the ecological importance of cyanobacteria through geological time.

Biomarkers↗
PubMed2007

Light stimulates growth of proteorhodopsin-containing marine Flavobacteria.

Proteorhodopsins are bacterial light-dependent proton pumps. Their discovery within genomic material from uncultivated marine bacterioplankton caused considerable excitement because it indicated a potential phototrophic function within these organisms, which had previously been considered strictly chemotrophic. Subsequent studies established that sequences encoding proteorhodopsin are broadly distributed throughout the world's oceans. Nevertheless, the role of proteorhodopsins in native marine bacteria is still unknown. Here we show, from an analysis of the complete genomes of three marine Flavobacteria, that cultivated bacteria in the phylum Bacteroidetes, one of the principal components of marine bacterioplankton, contain proteorhodopsin. Moreover, growth experiments in both natural and artificial seawater (low in labile organic matter, which is typical of the world's oceans) establish that exposure to light results in a marked increase in the cell yield of one such bacterium (Dokdonia sp. strain MED134) when compared with cells grown in darkness. Thus, our results show that the phototrophy conferred by proteorhodopsin can provide critical amounts of energy, not only for respiration and maintenance but also for active growth of marine bacterioplankton in their natural environment.

Amino Acid Sequence↗
PubMed1999

Reduction of (per)chlorate by a novel organism isolated from paper mill waste.

As part of a study on the microbiology of chlorate reduction, several new dissimilatory chlorate-reducing bacteria were isolated from a broad diversity of environments. One of these, strain CKB, was selected for a more complete characterization. Strain CKB was enriched and isolated from paper mill waste with acetate as the sole electron donor and chlorate as the sole electron acceptor. Strain CKB is a completely oxidizing, non-fermentative, Gram-negative, facultative anaerobe. Cells of strain CKB are 0.5 x 2 microm and are highly motile, with a single polar flagellum. In addition to acetate, strain CKB can use propionate, butyrate, lactate, succinate, fumarate, malate or yeast extract as electron donors, with chlorate as the sole electron acceptor. Strain CKB can also couple chlorate reduction to the oxidation of ferrous iron, sulphide, or the reduced form of the humic substances analogue 2,6-anthrahydroquinone disulphonate. Fe(II) is oxidized to insoluble amorphous Fe(II) oxide, whereas sulphide is oxidized to elemental sulphur. Growth is not associated with this metabolism, even when small quantities of acetate are added as a potential carbon source. In addition to chlorate, strain CKB can also couple acetate oxidation to the reduction of oxygen or perchlorate. Chlorate is completely reduced to chloride. Strain CKB has an optimum temperature of 35 degrees C, a pH optimum of 7.5 and a salinity optimum of 1% NaCl. Strain CKB can grow in chlorate and perchlorate concentrations of 80 or 20 mM respectively. Under anaerobic conditions, strain CKB can dismutate chlorite into chloride and O2, and is only the second organism shown to be capable of this metabolism. Oxidized minus reduced spectra of whole-cell suspensions of strain CKB showed absorbance maxima at 423, 523 and 552nm, which are indicative of the presence of c-type cytochrome(s). Analysis of the complete sequence of the 16S rDNA indicates that strain CKB is a member of the beta subclass of the Proteobacteria. The phototroph Rhodocyclus tenuis is the closest known relative. When tested, strain CKB could not grow by phototrophy and did not contain bacteriochlorophyll. Phenotypically and phylogenetically, strain CKB differs from all other described bacteria and represents the type strain of a new genus and species.

Betaproteobacteria↗