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Occurrence of facultative anoxygenic photosynthesis among filamentous and unicellular cyanobacteria.

Eleven of 21 cyanobacteria strains examined are capable of facultative anoxygenic photosynthesis, as shown by their ability to photoassimilate CO2 in the presence of Na2S, 3-(3,4-dichlorophenyl)-1,1-dimethylurea and 703-nm light. These include different cyanobacterial types (filamentous and unicellular) of different growth histories (aerobic, anaerobic, and marine and freshwater). Oscillatoria limnetica, Aphanothece halophytica (7418), and Lyngbya (7104) have different optimal concentrations of Na2S permitting CO2 photoassimilation, above which the rate decreases: 3.5, 0.7, and 0.1 mM, respectively. In A. halophytica, for each CO2 molecule photoassimilated two sulfide molecules are oxidized to elemental sulfur, which is excreted from the cells. The ecological and evolutionary significance of anoxygenic photosynthesis in the cyanobacteria is discussed.

Aerobiosis

Hydrogen metabolism in the facultative anoxygenic cyanobacteria (blue-green algae) Oscillatoria limnetica and Aphanothece halophytica.

Two facultative anoxygenic photoautotrophic cyanobacteria, Oscillatoria limnetica and Aphanothece halophytica were found capable of CO2 photoassimilation using molecular hydrogen as electron donor in a photosystem I driven reaction. A. halophytica was also capable of evolving hydrogen from Na-dithionite reduced methylviologen in a light independent reaction.

Anaerobiosis

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

Mining thermophile photosynthesis genes: a synthetic operon expressing Chloroflexota species reaction center genes in Rhodobacter sphaeroides.

Photosynthesis is the foundation of the vast majority of life systems, and therefore the most important bioenergetic process on earth, and the greatest diversity in photosynthetic systems are found in microorganisms. However, understanding of the biophysical and biochemical processes that transduce light to chemical energy has derived from the relatively small subset of proteins from microbes that are amenable to cultivation, in contrast to the huge number of microbial DNA sequences encoding proteins that catalyze the initial photochemical reactions that has been deposited in databases, such as from metagenomics. We describe the use of a Rhodobacter sphaeroides laboratory strain for expression of heterologous photosynthesis genes to demonstrate the feasibility of mining this resource, focusing on hot spring Chloroflexota gene sequences. Using a synthetic operon of genes, we produced a photochemically active complex of reaction center proteins in our biological system. We also present bioinformatic analyses of anoxygenic type II reaction center sequences from metagenomic samples collected from hot (42-90° C) springs available through the JGI IMG database, to generate a resource of diverse sequences that potentially are adapted to photosynthesis at such temperatures. These data provide a view into the natural diversity of anoxygenic photosynthesis, through a lens focused on high-temperature environments. The approach we took to express such genes can be applied for potential biotechnology purposes as well as for studies of fundamental catalytic properties of these heretofore inaccessible protein complexes.

Chloroflexota

Sulfide inhibition of photosystem II in cyanobacteria (blue-green algae) and tobacco chloroplasts.

The present study shows that in the presence of 600 nm light, sulfide acts as a specific inhibitor of photosynthetic electron transport between water and Photosystem II in the cyanobacteria Aphanothece halophytica and Synechococcus 6311 as well as in tobacco chloroplasts. In the presence of 600 nm light sulfied affects the fast fluorescence transients as does a low concentration (10 mM) of hydroxylamine; the fluorescence yield decreases in the presence of either chemical and can be restored by the addition of 3-(3,4-dichlorophenyl)-1,1-dimethylurea. In chloroplasts, however, NH2OH, an electron donor at high concentrations (40 mM), relieves the sulfide effect. In the dark, sulfide affects the cyanobacterial fluorescence transients through decrease of oxygen tension. The fluorescence yield increases in a similar pattern to that observed under nitrogen flushing. Upon omission of sulfide in A. halophytica, the characteristic aerobic fluorescence transients return, consistent with the ease of alternation between oxygenic and sulfide-dependent anoxygenic photosynthesis in many cyanobacteria.

Aerobiosis

Illuminating the coevolution of photosynthesis and Bacteria.

Life harnessing light energy transformed the relationship between biology and Earth-bringing a massive flux of organic carbon and oxidants to Earth's surface that gave way to today's organotrophy- and respiration-dominated biosphere. However, our understanding of how life drove this transition has largely relied on the geological record; much remains unresolved due to the complexity and paucity of the genetic record tied to photosynthesis. Here, through holistic phylogenetic comparison of the bacterial domain and all photosynthetic machinery (totally spanning >10,000 genomes), we identify evolutionary congruence between three independent biological systems-bacteria, (bacterio)chlorophyll-mediated light metabolism (chlorophototrophy), and carbon fixation-and uncover their intertwined history. Our analyses uniformly mapped progenitors of extant light-metabolizing machinery (reaction centers, [bacterio]chlorophyll synthases, and magnesium-chelatases) and enzymes facilitating the Calvin-Benson-Bassham cycle (form I RuBisCO and phosphoribulokinase) to the same ancient Terrabacteria organism near the base of the bacterial domain. These phylogenies consistently showed that extant phototrophs ultimately derived light metabolism from this bacterium, the last phototroph common ancestor (LPCA). LPCA was a non-oxygen-generating (anoxygenic) phototroph that already possessed carbon fixation and two reaction centers, a type I analogous to extant forms and a primitive type II. Analyses also indicate chlorophototrophy originated before LPCA. We further reconstructed evolution of chlorophototrophs/chlorophototrophy post-LPCA, including vertical inheritance in Terrabacteria, the rise of oxygen-generating chlorophototrophy in one descendant branch near the Great Oxidation Event, and subsequent emergence of Cyanobacteria. These collectively unveil a detailed view of the coevolution of light metabolism and Bacteria having clear congruence with the geological record.

Photosynthesis

Short-term virus-host interactions and functional dynamics in recently deglaciated Antarctic tundra soils.

Long-term chronosequence studies have shown that, as glaciers retreat, newly exposed soils become colonized through primary succession. To determine the key drivers of this process and their vulnerability to climate change, the short-term responses of these pioneering microbial communities also need to be elucidated. Here, we investigated how the taxonomic and functional structure of microbial communities, including viruses, changed over a 7-year period in an Antarctic glacier forefield. Using metagenomics and metatranscriptomics we assessed the influence of both abiotic and biotic factors on these communities. Our results revealed a highly heterogeneous bacteria-dominated microbial community, with Pseudomonas as the most abundant genus, followed by Lysobacter, Devosia, Cellulomonas, and Brevundimonas. This community exhibited the capacity for aerobic anoxygenic phototrophy, carbon and nitrogen fixation, and sulfur cycling, processes vital for survival in nutrient-poor environments. 52 high-quality metagenome-assembled genomes (MAGs) were recovered, representing both transient and cosmopolitan taxa, some of which were able to rapidly respond to environmental changes. A diverse and highly dynamic collection of lytic and temperate viruses was identified across all samples, with high clonal viral genomes typically detected in only one of the eight samples analyzed. Metatranscriptomic analyses confirmed the activity of lytic viruses, while prophage genomes featured much lower expression levels. Prophages appeared to influence host fitness through the expression of genes encoding membrane transporters. Additionally, the abundance of genes linked to antimicrobial compound synthesis and resistance, along with antiphage defense systems, highlights the importance of biotic interactions in driving microbial community succession and shaping short-term responses to environmental fluctuations.

Antarctica

Alleviation of CO2-Induced Reductions in Tomato Photosynthesis Under Deficit Irrigation by Purple Nonsulfur Photosynthetic Bacteria.

The stimulatory effect of elevated CO2 (eCO2) on photosynthesis in most C3 crops under water deficit often declines over time due to photosynthetic acclimation. An exception occurs in plants inoculated with symbiotic nitrogen-fixing bacteria. Photosynthetic bacteria (PSB), specifically anoxygenic purple nonsulfur bacteria (Rhodopseudomonas palustris in this study), a group of nitrogen-fixing bacteria, are effective in enhancing crop photosynthesis. Therefore, this study investigated the synergistic effects of PSB and eCO2 in alleviating the effects of deficit irrigation and enhancing photosynthetic capacity in tomato plants during prolonged exposure. Our results showed that photosynthetic efficiency was significantly reduced in noninoculated plants under eCO2, and this reduction was more pronounced under water deficit. Proteomic analysis revealed that in eCO2-treated plants, the downregulation of cell wall proteins increased mesophyll resistance to CO2 diffusion, while the suppression of the photosynthetic apparatus impaired electron transport capacity, ultimately reducing CO2 assimilation efficiency. In contrast, these negative effects were alleviated by PSB inoculation. PSB promoted the upregulation of proteins involved in photosynthesis under deficit irrigation, as well as proteins related to chlorophyll biosynthesis, components of photosystem I and II, and light-harvesting complex proteins. These proteins contributed to improved photosynthetic efficiency during deficit irrigation and photosynthetic acclimation. Physiological analyses further confirmed that PSB inoculation enhanced nitrogen content, electron transport capacity, chlorophyll biosynthesis, and overall photosynthetic performance under eCO2 and deficit irrigation, resulting in improved plant growth. These findings suggest that PSB inoculation is a promising strategy to sustain and enhance the CO2 fertilization effect on crop productivity under water-limited conditions.

Photosynthesis

Induction of anaerobic, photoautotrophic growth in the cyanobacterium Oscillatoria limnetica.

Anaerobic photoautotrophic growth of the cyanobacterium Oscillatoria limnetica was demonstrated under nitrogen in the presence of 3-(3,4-dichlorophenyl)-1,1-dimethylurea (5micron), a constant concentration of Na2S (2.5 mM), and constant pH (7.3). The photoanaerobic growth rate (2 days doubling time) was similar to that obtained under oxygenic photoautotrophic growth conditions. The potential of oxygenic photosynthesis is constitutive in the cells; that of anoxygenic photosynthesis is rapidly (2 h) induced in the presence of Na2S in the light in a process requiring protein synthesis. The facultative anaerobic phototrophic growth physiology exhibited by O. limnetica would seem to represent an intermediate physiological pattern between the obligate anaerobic one of photosynthetic bacteria and the oxygenic one of eucaryotic algae.

Aerobiosis