A niche for cyanobacteria containing chlorophyll d

Kühl, Michael; Chen, Min; Ralph, Peter J.; Schreiber, Ulrich; Larkum, Anthony W. D.

doi:10.1038/433820a

Cited by 192 publications

(150 citation statements)

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“…This is particularly critical when analyzing surface-associated microbial communities, where several studies of microbial mats Kunin et al, 2008) and sediments (Lü demann et al, 2000;Bö er et al, 2009) have shown strong shifts in microbial communities along biogeochemical gradients over minute spatial scales. Although microenvironmental analysis of corals (Kü hl et al, 1995), sponges (Hanna et al, 2005;Hoffmann et al, 2008) and ascidians (Kü hl and Larkum, 2002;Kü hl et al, 2005) have shown steep and dynamic microenvironmental conditions similar to biofilms and microbial mats, we are not aware of previous studies simultaneously mapping microbial diversity and fine-scale microenvironmental conditions in such organisms.…”

Section: Introductionmentioning

confidence: 97%

“…For example, Schmidt et al (2005) reported the production of bioactive cyclic peptides, patellamides, in the symbiotic prochlorophytic cyanobacterium Prochloron spp., which is found in large quantities within the cloacal cavity of the didemnid ascidian Lissoclinum patella (Schmidt et al, 2005), whereas others have reported patellamide production in L. patella itself (Degnan et al, 1989;Sings and Rinehart, 1996;Salomon and Faulkner, 2002). Another unique cyanobacterium, Acaryochloris marina, grows in biofilms on the underside of didemnid ascidians, where it uses chlorophyll (Chl) d to sustain its photosynthesis using near-infrared radiation (NIR; Kü hl et al, 2005). The A. marina type strain MBIC11017, originally isolated from L. patella, was hereafter sequenced and revealed a genome of unusually large size (Swingley et al, 2008).…”

Section: Introductionmentioning

confidence: 99%

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Microbial diversity of biofilm communities in microniches associated with the didemnid ascidian Lissoclinum patella

et al. 2011

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We assessed the microbial diversity and microenvironmental niche characteristics in the didemnid ascidian Lissoclinum patella using 16S rRNA gene sequencing, microsensor and imaging techniques. L. patella harbors three distinct microbial communities spatially separated by few millimeters of tunic tissue: (i) a biofilm on its upper surface exposed to high irradiance and O 2 levels, (ii) a cloacal cavity dominated by the prochlorophyte Prochloron spp. characterized by strong depletion of visible light and a dynamic chemical microenvironment ranging from hyperoxia in light to anoxia in darkness and (iii) a biofilm covering the underside of the animal, where light is depleted of visible wavelengths and enriched in near-infrared radiation (NIR). Variable chlorophyll fluorescence imaging demonstrated photosynthetic activity, and hyperspectral imaging revealed a diversity of photopigments in all microhabitats. Amplicon sequencing revealed the dominance of cyanobacteria in all three layers. Sequences representing the chlorophyll d containing cyanobacterium Acaryochloris marina and anoxygenic phototrophs were abundant on the underside of the ascidian in shallow waters but declined in deeper waters. This depth dependency was supported by a negative correlation between A. marina abundance and collection depth, explained by the increased attenuation of NIR as a function of water depth. The combination of microenvironmental analysis and fine-scale sampling techniques used in this investigation gives valuable first insights into the distribution, abundance and diversity of bacterial communities associated with tropical ascidians. In particular, we show that microenvironments and microbial diversity can vary significantly over scales of a few millimeters in such habitats; which is information easily lost by bulk sampling.

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Section: Introductionmentioning

confidence: 97%

Section: Introductionmentioning

confidence: 99%

Microbial diversity of biofilm communities in microniches associated with the didemnid ascidian Lissoclinum patella

et al. 2011

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“…Acaryochloris ecotypes have been found in marine environments in close association with other oxygenic phototrophs such as Prochloron (associate with colonial ascidians) (3,5,10), eukaryotic macroalgae (11,12), and in a microbial mat in the Salton Sea, a saline and highly eutrophic California lake (13). In each environment, the photosynthetically available radiation is likely completely used by organisms that absorb light using Chl a and/or Chl b.…”

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confidence: 99%

Niche adaptation and genome expansion in the chlorophyll d -producing cyanobacterium Acaryochloris marina

Swingley

Chen

Cheung³

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

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Acaryochloris marina is a unique cyanobacterium that is able to produce chlorophyll d as its primary photosynthetic pigment and thus efficiently use far-red light for photosynthesis. Acaryochloris species have been isolated from marine environments in association with other oxygenic phototrophs, which may have driven the niche-filling introduction of chlorophyll d. To investigate these unique adaptations, we have sequenced the complete genome of A. marina. The DNA content of A. marina is composed of 8.3 million base pairs, which is among the largest bacterial genomes sequenced thus far. This large array of genomic data is distributed into nine single-copy plasmids that code for >25% of the putative ORFs. Heavy duplication of genes related to DNA repair and recombination (primarily recA) and transposable elements could account for genetic mobility and genome expansion. We discuss points of interest for the biosynthesis of the unusual pigments chlorophyll d and ␣-carotene and genes responsible for previously studied phycobilin aggregates. Our analysis also reveals that A. marina carries a unique complement of genes for these phycobiliproteins in relation to those coding for antenna proteins related to those in Prochlorococcus species. The global replacement of major photosynthetic pigments appears to have incurred only minimal specializations in reaction center proteins to accommodate these alternate pigments. These features clearly show that the genus Acaryochloris is a fitting candidate for understanding genome expansion, gene acquisition, ecological adaptation, and photosystem modification in the cyanobacteria.comparative microbial genomics ͉ photosynthesis ͉ oxygenic phototrophs ͉ evolution

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“…The textbook concept that oxygenic phototrophs primarily use radiation in the visible range (400-700 nm) has been challenged by several findings of unique cyanobacteria and chlorophylls (Chl) over the past two decades (Miyashita et al, 1996;Chen et al, 2010;Croce and van Amerongen, 2014) Unicellular cyanobacteria in the genus Acaryochloris primarily employ Chl d for oxygenic photosynthesis at 700-720 nm (Miyashita et al, 1996) and thrive in shaded habitats with low levels of visible light but replete of near-infrared radiation (NIR, 4700 nm, Kü hl et al, 2005;Behrendt et al, 2011Behrendt et al, , 2012. Furthermore, Chl f was recently discovered in filamentous (Chen et al, 2010;Airs et al, 2014;Gan et al, 2014) and unicellular cyanobacteria (Miyashita et al, 2014), enabling light harvesting even further into the NIR region up to B740 nm, often aided by employing additional far-red light-absorbing pigments such as Chl d and phycobiliproteins (Gan et al, 2014).…”

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Chlorophyll f-driven photosynthesis in a cavernous cyanobacterium

et al. 2015

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Chlorophyll (Chl) f is the most recently discovered chlorophyll and has only been found in cyanobacteria from wet environments. Although its structure and biophysical properties are resolved, the importance of Chl f as an accessory pigment in photosynthesis remains unresolved. We found Chl f in a cyanobacterium enriched from a cavernous environment and report the first example of Chl f-supported oxygenic photosynthesis in cyanobacteria from such habitats. Pigment extraction, hyperspectral microscopy and transmission electron microscopy demonstrated the presence of Chl a and f in unicellular cyanobacteria found in enrichment cultures. Amplicon sequencing indicated that all oxygenic phototrophs were related to KC1, a Chl f-containing cyanobacterium previously isolated from an aquatic environment. Microsensor measurements on aggregates demonstrated oxygenic photosynthesis at 742 nm and less efficient photosynthesis under 768-and 777-nm light probably because of diminished overlap with the absorption spectrum of Chl f and other far-red absorbing pigments. Our findings suggest the importance of Chl f-containing cyanobacteria in terrestrial habitats.

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A niche for cyanobacteria containing chlorophyll d

Cited by 192 publications

References 9 publications

Microbial diversity of biofilm communities in microniches associated with the didemnid ascidian Lissoclinum patella

Microbial diversity of biofilm communities in microniches associated with the didemnid ascidian Lissoclinum patella

Niche adaptation and genome expansion in the chlorophyll d -producing cyanobacterium Acaryochloris marina

Chlorophyll f-driven photosynthesis in a cavernous cyanobacterium

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