Galdieria sulphuraria

Galdieria sulphuraria is an extremophilic unicellular species of red algae. It is the type species of the genus Galdieria.[2] It is known for its broad metabolic capacities, including photosynthesis and heterotrophic growth on over 50 different extracellular carbon sources. The members of the class Cyanidiophyceae are among the most acidophilic known photosynthetic organisms, and the growth conditions of G. sulphuraria – pH between 0 and 4, and temperatures up to 56 °C – are among the most extreme known for eukaryotes. Analysis of its genome suggests that its thermoacidophilic adaptations derive from horizontal gene transfer from archaea and bacteria, another rarity among eukaryotes.[3]

Galdieria sulphuraria
Scientific classification Edit this classification
(unranked): Archaeplastida
Division: Rhodophyta
Class: Cyanidiophyceae
Order: Cyanidiales
Family: Galdieriaceae
Genus: Galdieria
Species:
G. sulphuraria
Binomial name
Galdieria sulphuraria
Merola et al., 1981[1]

History and taxonomy

Published descriptions of thermoacidophilic unicellular algae date to the mid-19th century. The earliest description of an organism corresponding to the modern G. sulphuraria was published in 1899 by an Italian scientist, A. Galdieri, who gave it the name Pleurococcus sulphurarius. The taxonomy of thermoacidophilic algae was revised in 1981, which introduced the genus Galdieria and gave the organism its modern designation.[1][4] G. sulphuraria is the type species for this genus.[1][2]

The group to which G. sulphuraria belongs, the Cyanidiophyceae, is the most deeply branching subgroup of the rhodophyta (red algae), meaning they were the earliest to diverge in the evolutionary history of this group.[5]

Metabolism

G. sulphuraria is noted for its extreme metabolic flexibility: it is capable of photosynthesis and can also grow heterotrophically on a wide variety of carbon sources, including diverse carbohydrates. Over 50 different carbon sources that support growth have been reported.[6][7][8] Careful measurements of its growth patterns under laboratory conditions suggest that it is not a true mixotroph capable of using both energy sources at the same time; rather, it prefers heterotrophic growth conditions and downregulates photosynthesis after extended exposure to extracellular carbon sources.[9] Analysis of the G. sulphuraria photosystem I complex, a key photosynthetic component, suggests a structure intermediate between the homologous complexes in cyanobacteria and plants.[8]

Although most red algae use floridean starch as a storage glucan, G. sulphuraria uses a highly unusual form of glycogen which is among the most highly branched glycogens known, has very short branch lengths, and forms particles of unusually low molecular weight. These properties are believed to be metabolic adaptations to extreme environmental conditions, although the precise mechanism is unclear.[10]

Habitat and ecology

G. sulphuraria is unusual for a eukaryote in being thermoacidophilic – that is, capable of growing at both high temperature and low pH. It grows well in a pH range of 0–4 and at temperatures up to 56 °C,[9] close to the approximately 60 °C sometimes cited as the likely maximum for eukaryotic life.[11][12] It is also highly tolerant of high salt concentrations and of toxic metals. It is found in naturally acidic hot springs, in solfataric environments, and in polluted environments;[3] It is also found in endolithic ecosystems, where light is scarce and its heterotrophic metabolic capacities are particularly important.[13][14][15] Laboratory tests indicate that it is capable of actively acidifying its environment.[9]

Genome

The G. sulphuraria genome contains evidence of extensive horizontal gene transfer (HGT) from thermoacidophilic archaea and bacteria, explaining the origin of its adaptation to this environment. At least 5% of its proteome is likely to be derived from HGT.[3] This is highly unusual for a eukaryote; relatively few well-substantiated examples exist of HGT from prokaryotes to eukaryotes.[16]

The genome of its mitochondria is also exceptionally small and has a very high GC skew, while the genome of its plastids is of normal size but contains an unusual number of stem-loop structures. Both of these properties are proposed to be adaptations for the organism's polyextremophilic environment.[17] By comparison to Cyanidioschyzon merolae – a unicellular thermoacidophilic red alga that is obligately photoautotrophic – the G. sulphuraria genome contains a large number of genes associated with carbohydrate metabolism and cross-membrane transport.[18]

Biotechnology

Because of its ability to tolerate extreme environments and grow under a wide variety of conditions, G. sulphuraria has been considered for use in bioremediation projects. For example, it has been tested for the ability to recover precious metals,[19] recover rare-earth metals,[20] and remove phosphorus and nitrogen[21] from various waste streams.

It is also an interesting source of proteins and especially phycocianin. The phycocianin produced by this specie is interesting since it is thermoresistant and acidotestant, two interesting properties for food application.

References
  1. Merola, Aldo; Castaldo, Rosa; Luca, Paolo De; Gambardella, Raffaele; Musacchio, Aldo; Taddei, Roberto (1981). "Revision of Cyanidium caldarium. Three species of acidophilic algae". Giornale Botanico Italiano. 115 (4–5): 189–195. doi:10.1080/11263508109428026.
  2. Guiry, M.D.; Guiry, G.M. "Galdieria sulphuraria". AlgaeBase. World-wide electronic publication, National University of Ireland, Galway.
  3. Schönknecht, G; Chen, WH; Ternes, CM; Barbier, GG; Shrestha, RP; Stanke, M; Bräutigam, A; Baker, BJ; Banfield, JF; Garavito, RM; Carr, K; Wilkerson, C; Rensing, SA; Gagneul, D; Dickenson, NE; Oesterhelt, C; Lercher, MJ; Weber, AP (8 March 2013). "Gene transfer from bacteria and archaea facilitated evolution of an extremophilic eukaryote". Science. 339 (6124): 1207–10. Bibcode:2013Sci...339.1207S. doi:10.1126/science.1231707. PMID 23471408. S2CID 5502148.
  4. Albertano, P.; Ciniglia, C.; Pinto, G.; Pollio, A. (2000). "The taxonomic position of Cyanidium, Cyanidioschyzon and Galdieria: an update". Hydrobiologia. 433 (1/3): 137–143. doi:10.1023/A:1004031123806. S2CID 11634959.
  5. Yoon, Hwan Su; Muller, Kirsten M.; Sheath, Robert G.; Ott, Franklyn D.; Bhattacharya, Debashish (April 2006). "Defining the Major Lineages of Red Algae (Rhodophyta)1". Journal of Phycology. 42 (2): 482–492. doi:10.1111/j.1529-8817.2006.00210.x. S2CID 27377549.
  6. Weber, AP; Oesterhelt, C; Gross, W; Bräutigam, A; Imboden, LA; Krassovskaya, I; Linka, N; Truchina, J; Schneidereit, J; Voll, H; Voll, LM; Zimmermann, M; Jamai, A; Riekhof, WR; Yu, B; Garavito, RM; Benning, C (May 2004). "EST-analysis of the thermo-acidophilic red microalga Galdieria sulphuraria reveals potential for lipid A biosynthesis and unveils the pathway of carbon export from rhodoplasts" (PDF). Plant Molecular Biology. 55 (1): 17–32. doi:10.1007/s11103-004-0376-y. PMID 15604662. S2CID 35848466.
  7. Oesterhelt, C; Klocke, S; Holtgrefe, S; Linke, V; Weber, AP; Scheibe, R (September 2007). "Redox regulation of chloroplast enzymes in Galdieria sulphuraria in view of eukaryotic evolution". Plant and Cell Physiology. 48 (9): 1359–73. doi:10.1093/pcp/pcm108. PMID 17698881.
  8. Vanselow, C; Weber, AP; Krause, K; Fromme, P (January 2009). "Genetic analysis of the Photosystem I subunits from the red alga, Galdieria sulphuraria". Biochimica et Biophysica Acta (BBA) - Bioenergetics. 1787 (1): 46–59. doi:10.1016/j.bbabio.2008.10.004. PMID 19007746.
  9. Oesterhelt, C; Schmälzlin, E; Schmitt, JM; Lokstein, H (August 2007). "Regulation of photosynthesis in the unicellular acidophilic red alga Galdieria sulphuraria". The Plant Journal. 51 (3): 500–11. doi:10.1111/j.1365-313x.2007.03159.x. PMID 17587234.
  10. Martinez-Garcia, Marta; Stuart, Marc C.A.; van der Maarel, Marc J.E.C (August 2016). "Characterization of the highly branched glycogen from the thermoacidophilic red microalga Galdieria sulphuraria and comparison with other glycogens" (PDF). International Journal of Biological Macromolecules. 89: 12–18. doi:10.1016/j.ijbiomac.2016.04.051. PMID 27107958.
  11. Rothschild, Lynn J.; Mancinelli, Rocco L. (22 February 2001). "Life in extreme environments". Nature. 409 (6823): 1092–1101. Bibcode:2001Natur.409.1092R. doi:10.1038/35059215. PMID 11234023. S2CID 529873.
  12. Weber, AP; Horst, RJ; Barbier, GG; Oesterhelt, C (2007). "Metabolism and metabolomics of eukaryotes living under extreme conditions". International Review of Cytology. 256: 1–34. doi:10.1016/S0074-7696(07)56001-8. ISBN 9780123737007. PMID 17241903.
  13. Gross, Wolfgang; Küver, Jan; Tischendorf, Gilbert; Bouchaala, Nicolas; Büsch, Wilhelm (February 1998). "Cryptoendolithic growth of the red alga in volcanic areas". European Journal of Phycology. 33 (1): 25–31. doi:10.1080/09670269810001736503.
  14. Gross, W.; Oesterhelt, Christine (November 1999). "Ecophysiological Studies on the Red Alga Isolated from Southwest Iceland". Plant Biology. 1 (6): 694–700. doi:10.1111/j.1438-8677.1999.tb00282.x.
  15. Walker, JJ; Spear, JR; Pace, NR (21 April 2005). "Geobiology of a microbial endolithic community in the Yellowstone geothermal environment". Nature. 434 (7036): 1011–4. Bibcode:2005Natur.434.1011W. doi:10.1038/nature03447. PMID 15846344. S2CID 4408407.
  16. Schönknecht, G; Weber, AP; Lercher, MJ (January 2014). "Horizontal gene acquisitions by eukaryotes as drivers of adaptive evolution". BioEssays. 36 (1): 9–20. doi:10.1002/bies.201300095. PMID 24323918. S2CID 3809570.
  17. Jain, K; Krause, K; Grewe, F; Nelson, GF; Weber, AP; Christensen, AC; Mower, JP (30 December 2014). "Extreme features of the Galdieria sulphuraria organellar genomes: a consequence of polyextremophily?". Genome Biology and Evolution. 7 (1): 367–80. doi:10.1093/gbe/evu290. PMC 4316638. PMID 25552531.
  18. Barbier, G; Oesterhelt, C; Larson, MD; Halgren, RG; Wilkerson, C; Garavito, RM; Benning, C; Weber, AP (February 2005). "Comparative genomics of two closely related unicellular thermo-acidophilic red algae, Galdieria sulphuraria and Cyanidioschyzon merolae, reveals the molecular basis of the metabolic flexibility of Galdieria sulphuraria and significant differences in carbohydrate metabolism of both algae". Plant Physiology. 137 (2): 460–74. doi:10.1104/pp.104.051169. PMC 1065348. PMID 15710685.
  19. Ju, X; Igarashi, K; Miyashita, S; Mitsuhashi, H; Inagaki, K; Fujii, S; Sawada, H; Kuwabara, T; Minoda, A (July 2016). "Effective and selective recovery of gold and palladium ions from metal wastewater using a sulfothermophilic red alga, Galdieria sulphuraria". Bioresource Technology. 211: 759–64. doi:10.1016/j.biortech.2016.01.061. PMID 27118429.
  20. Minoda, A; Sawada, H; Suzuki, S; Miyashita, S; Inagaki, K; Yamamoto, T; Tsuzuki, M (February 2015). "Recovery of rare earth elements from the sulfothermophilic red alga Galdieria sulphuraria using aqueous acid". Applied Microbiology and Biotechnology. 99 (3): 1513–9. doi:10.1007/s00253-014-6070-3. PMID 25283836. S2CID 253774729.
  21. Selvaratnam, T; Pegallapati, AK; Montelya, F; Rodriguez, G; Nirmalakhandan, N; Van Voorhies, W; Lammers, PJ (March 2014). "Evaluation of a thermo-tolerant acidophilic alga, Galdieria sulphuraria, for nutrient removal from urban wastewaters". Bioresource Technology. 156: 395–9. doi:10.1016/j.biortech.2014.01.075. PMID 24582952.
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