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Acaryochloris Marina Syed Lal Badshah1,2*, Yahia Mabkhot3* and Salim S

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Acaryochloris Marina Syed Lal Badshah1,2*, Yahia Mabkhot3* and Salim S Badshah and Mabkhot Biol Res (2017) 50:16 DOI 10.1186/s40659-017-0120-0 Biological Research REVIEW Open Access Photosynthesis at the far‑red region of the spectrum in Acaryochloris marina Syed Lal Badshah1,2*, Yahia Mabkhot3* and Salim S. Al‑Showiman3* Abstract Acaryochloris marina is an oxygenic cyanobacterium that utilizes far-red light for photosynthesis. It has an expanded genome, which helps in its adaptability to the environment, where it can survive on low energy photons. Its major light absorbing pigment is chlorophyll d and it has α-carotene as a major carotenoid. Light harvesting antenna includes the external phycobilin binding proteins, which are hexameric rods made of phycocyanin and allophyco‑ cyanins, while the small integral membrane bound chlorophyll binding proteins are also present. There is specifc chlorophyll a molecule in both the reaction center of Photosystem I (PSI) and PSII, but majority of the reaction center consists of chlorophyll d. The composition of the PSII reaction center is debatable especially the role and position of chlorophyll a in it. Here we discuss the photosystems of this bacterium and its related biology. Keywords: Oxygenic photosynthesis, Acaryochloris species, Chlorophyll d, Photosystem, Phycobillisomes, P740 Background through which Chl a can be converted into Chl d without In 1996 a new oxygenic photosynthetic cyanobacterium utilizing any enzyme [4, 5]. Te presence of this formyl was discovered, which contains chlorophyll d as the major group causes the Qy absorption to red shift by ≈30 nm pigment [1]. Tis organism has a 95% chlorophyll d along in vitro [6] and ≈40 nm in vivo [6]. As a result there is with 5% chlorophyll a in its photosynthetic structures. 0.1 V lower electronic energy gap between the ground and Te main diference between chlorophyll a and d is the lower excited state [7, 8]. Te molar extinction coefcient 3 −1 −1 side chain attached at carbon three position of the chlorin of chlorophyll d is 63.68 × 10 L mol ­A697 nm cm in ring [2]. In chlorophyll d, it is a formyl group instead of 100% methanol [9]. Te protein binding properties of Chl a vinyl group (Fig. 1) [1, 2]. Oxidation of the 3-vinyl side d are similar to that of Chl a [10] and that is why Chl d can chain of chlorophyll a to 3-formyl group may leads to the function as both a light harvesting pigment in the antenna formation of chlorophyll d however the enzyme involved as well as a redox active cofactor in the reaction center is not yet known and it is possibly diferent from chloro- (RC) of PSI and PSII in A. marina [11, 12]. Tere are few phyllide a oxidase (CAO). CAO normally converts Chl reviews [13–16] available on A. marina but still there is a a to Chl b. Te 18O labeling studies have revealed that need to further reviewed its photosynthesis as research is the insertion of formyl group in Chl d involves an oxy- going on and there are a number of disagreements on the genase enzyme [3]. Further, the oxygen atom in the for- location of specifc cofactors in its reaction centers. Te myl group of Chl d has its origin from molecular oxygen search for the presence of other chlorophyll d containing and Chl a is the possible biosynthetic antecedent of Chl cyanobacteria is also continuous and currently Martinez- d [3]. Tere are a number of chemical methods available Garcia et al. [17] found chlorophyll d from the HPLC analysis of phototrophic epibiotic community attached with ascidian Cystodytes dellechiajei. However from the *Correspondence: [email protected]; [email protected]; denaturing gradient gel electrophoresis they did not fnd [email protected] 1 Department of Chemistry, Islamia College University Peshawar, A. marina in their bacterial samples. Tere may be other Peshawar 25120, Khyber Pakhtunkhwa, Pakistan types of cyanobacteria which may utilize chlorophyll d 3 Department of Chemistry, College of Science, King Saud University, [17]. For example, the production of Chl d was recently Riyad, Saudi Arabia Full list of author information is available at the end of the article reported in cyanobacterium called Chlorogloeopsis © The Author(s) 2017. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/ publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Badshah and Mabkhot Biol Res (2017) 50:16 Page 2 of 9 Fig. 1 Molecular structure; carbon numbering and specifc groups in chlorophyll a and d molecules fritschii, when grown under near infra-red light condi- ongoing [25]. Tese far-red light absorbing cyanobacte- tions [18]. Sea squirts (ascidians) from the Bahamas ria loves to colonize the invertebrate ascidian Lissoclinum showed some new cyanobacteria that have chlorophyll d patella which are present in diferent layers in shallow and their 16S rRNA content analysis showed close resem- water. Tus the ascidian are reservoirs for collection of A. blance with Acaryochloris [19]. A. marina harvest the far marina sample isolation [26]. Kühl and co-workers have red light with its chlorophyll d better [20] and live in sym- developed a new TaqMan-centered quantitative PCR biotic relationship with other photosynthetic bacteria like (qPCR) assay for fast screening of environmental samples Prochloron, Eukaryotic macro-algae and diferent types of for identifcation of Acaryochloris species from diferent microbial mat in marine environment and also in Salton geographical locations. Te DNA samples of fve strains saline Lake of California where chlorophyll a and b absorb of A. marina, i.e., MBIC11017, CCMEE5410, HICR111A, most of the light [21]. Similarly a new specie has been CRS, and Awaji-1, displayed amplifcation productivities isolated from the great barrier reef of Australia, which is of more than 94%. Further based on this assay, in four diferent in several aspects from the already known spe- samples of crustose coralline algae gathered from moder- cies of Acaryochloris below crustose coralline algae from ate and humid regions, A. marina was present. Tus this endolithic habitat on coral reefs [22]. Te search for pho- assay is quick and highly efcient method for the detec- totrophic bacteria continued and these bacteria have been tion of Acaryochloris strains in diverse locations [25]. isolated from Antarctic rocks and limestones from his- torical places [23]. Tey have also been isolated from the Genomics coast of Republic of Palau where they live in close asso- A. marina is one of the cyanobacterium whose genome ciation with other cyanobacteria on Didemnid Ascidians has been fully sequenced [27]. Tere are 8.3 million and Sponge showing a diversity throughout the world base pairs (bp) and it is considered as the biggest pho- [24]. Acaryochloris is now a separate genus that contains tosynthetic bacterial genome sequenced so far [27]. Its seven diferent strains and the search for new strains is genomic data is spread into one large chromosome and Badshah and Mabkhot Biol Res (2017) 50:16 Page 3 of 9 nine single copy plasmids, which codes for more than Te main chromosomes also contain PBP related genes, 25% open reading frames (ORFs) [27]. Tis large genome these are the three copies of apcA and one copy of apcB makes A. marina a suitable organism to accommodate [27]. Te rest of PBP linked genes are located on pREB3 itself in variable environment with low light conditions. in an enormous number of gene clusters. A. marina has Te sequence comparisons showed that these plasmids a full complement of genes that encode the photosys- did not arise from recent duplication phenomena, but tems [27]. In its sequenced genome, the genes for psaI some of the plasmids have a good number of sequence are absent which is important protein for the stabiliza- area that are homologous. Most of the RNAs are encoded tion of PSI trimer. Tere are three copies of each psbA by the large single circular chromosome while the plas- (D1 subunit) and psbD (D2 subunit) of PSII protein genes mids encoded phycocyanin related genes, hydrogenase and are closely homologous to one another [27]. Te PSII genes, genes of the second alternate ATP synthase, and D1 and D2 subunits primary sequence are extremely well several metabolic enzymes. Te A. marina genome conserved like other cyanobacteria and the only signif- contains a huge number of genes that help in adaptive cant diference is that chlorophyll d replaces chlorophyll regulation of diferent biological activities. Tere are a a [27]. Further there are duplicated copies of psbU, psaK number of recA genes which are responsible for repair and psbE conserved genes on the plasmids of A. marina. and recombination enzymes so that the bacterium can In A. marina genome, most of the cytochrome b6f genes expand its genome by duplication of genes and in assimi- are present as a single copy with the exception of petH lation of foreign genes. From comparative analysis of and petJ genes [27]. Te new Acaryochloris species that several genomes, it has been hypothesized that species are isolated from Great Barrier Reef has 2% diferent 16S with expanded genomes are suitable for living in non- rRNA from the ones discovered earlier [19]. Te genetic competitive niche having low but comprehensive amount characterization of newly discovered species of Acary- of nutrients in nature [28]. Tis hypothesis holds true ochloris are in progress and their genomics show that for A.
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