In 1996, Miyashita et al. reported the discovery of an oxygenic photosynthetic prochlorophyte-like prokaryote predominantly containing the green pigment chlorophyll (Chl) d. The cyanobacterium was discovered living in a suspension of algae squeezed from a colonial ascidian (or sea squirt) Lissoclinum patella off the coast of the Palau Islands in the western Pacific Ocean [1]. The prokaryote was named Acaryochloris marina (hereby referred to as A. marina) Miyashita et Chihara gen. et sp. nov. by Miyashita et al. and has been listed as the strain MBIC 11017 in the Marine Biotechnology Institute Culture collection.

Interestingly, this species of cyanobacteria is thought to have been encountered 53 years prior to its discovery in 1996 by a pair of chemists called Winston M. Manning and Harold H. Strain in 1943, who presented the discovery of Chl d as a previously undiscovered green pigment of red algae [2]. It was suggested by some that Chl d could be a byproduct induced during pigment extraction and the subject of the origin of the new form of chlorophyll was left unresolved for just over half a century [3]. In fact, in 2004, Murakami et al. identified another strain of A. marina as an epiphyte on the thalli of the red alga Ahnfeltiopsis flabelliformis, which they named A. marina sp. strain Awaji. Murakami et al. also mentioned in their paper that the Awaji strain was not restricted to just Ahnfeltiopsis flabelliformis, but was found on other marine Rhodophyta, namely Callophyllis japonica and Carpopeltis prolifera [4].

In a recent paper by Larkum and Kühl [5], doubts were raised concerning the isolation of A. marina from within didemnid ascidians as presented by Miyashita et al. [1]. The main dispute from their investigations arose from the nature of the habitats of A. marina and the significance of it predominantly containing Chl d. Earlier in 2005, Kühl et al. discussed the niche-nature of A. marina characterised by its habitats and that it exploits near infrared radiation (NIR) by containing mainly Chl d which absorbs light in the far red-light region above 680 nm. In particular Kühl et al. presented ample evidence in their microphotometric survey of didemnid ascidians (Lissoclinum patella, Trididemnum paracyclops, Diplosoma similis and Diplosoma virens collected on the reef flat off Heron Island from the Great Barrier Reef) indicating A. marina-like cyanobacteria form biofilms on the underside of didemnid ascidians as opposed to being symbiotic within colonial ascidians. Kühl et al. also used fibre-optic microprobe measurements in D. virens to show that visible light is attenuated by the ascidian tissue, providing strong data to support an ideal niche habitat for A. marina [6]. Larkum and Kühl argue in [5] that the presence of A. marina-like cyanobacteria on the underside of Rhodophyta [4], which strongly deplete visible light and enhance NIR and the supporting evidence of the microphotometric survey [6] not only resolve the issue of the source concerning the initial discovery of Chl d by Manning and Strain [2], but also highlights these two niche habitats which allow far-red light through, to possibly be the original habitats of A. marina.

However, a further strain of A. marina, which has been denoted CCMEE 5410 (deposited at the University of Oregon Culture Collection of Microorganisms from Extreme Environments) was discovered free-living on an epilithic microbial mat on dyke-forming rip rap rock on the southern shore of the Salton Sea, a eutrophic and highly polluted, hypersaline lake [7]. Larkum and Kühl suggest this ability of A. marina-like cyanobacteria to exist under such extreme conditions supports the idea that A. marina-like cyanobacteria can exist in such different nutritional habitats as epiphytes on ascidians and on the underside of Rhodophyta. Currently there is no evidence to suggest that A. marina is not symbiotic within ascidians, although Larkum and Kühl appear doubtful suggesting the possibility of ingestion of A. marina by the ascidians by bioturbation in a restricted environment [5].

More recently it has been discovered that Acaryochloris species are also found not only on red, but also on green and brown algae [8]. De los Rios et al. also identified a putative endolithic strain of A. marina in granite rock fissures in continental Antarctica using phylogeny of the 16S rRNA gene [9].

References

1. Miyashita, H., H. Ikemoto, et al. (1996). Chlorophyll d as a major pigment. Nature 383: 402.

2. Manning, W. M. and H. H. Strain (1943). Chlorophyll d, a green pigment of red algae. J Biol Chem 151: 1-19.

3. Holt, A. S. (1961). Further evidence of the relation between 2-desvinyl-2-formyl-chlorophyll a and chlorophyll d. Can J Bot 39: 327-331.

4. Murakami, A., H. Miyashita, et al. (2004). Chlorophyll d in an epiphytic cyanobacterium of red algae. Science 303(5664): 1633.

5. Larkum, A. W. and M. Kuhl (2005). Chlorophyll d: the puzzle resolved. Trends Plant Sci 10(8): 355-7.

6. Kuhl, M., M. Chen, et al. (2005). Ecology: a niche for cyanobacteria containing chlorophyll d. Nature 433(7028): 820.

7. Miller, S. R., S. Augustine, et al. (2005). Discovery of a free-living chlorophyll d-producing cyanobacterium with a hybrid proteobacterial/cyanobacterial small-subunit rRNA gene. Proc Natl Acad Sci USA 102(3): 850-5.

8. Ohkubo S. et al. (2006) Molecular detection of epiphytic Acaryochloris spp. on marine macroalgae. Appl Environ Microbiol 72: 7912–7915.

9. de los Rios A., Grube M. et al. (2007) Ultrastructural and genetic characteristics of endolithic cyanobacterial biofilms colonizing Antarctic granite rocks. FEMS Microbiol Ecol 59(2):386-95.

MBIC Collection

Acaryochloris marina was isolated by Miyashita et al. and deposited in the Marine Biotechnology Institute Culture Collection, Japan.

Phototrophic Prokaryotes Sequencing Project

Acaryochloris marina MBIC11017 is one of four phototrophic prokaryotes selected for sequencing in this project. The Acaryochloris genome is currently being annotated.