Galdieria sulphuraria

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Galdieria sulphuraria
Fmicb-07-02022-g002-extr.jpg
A picture of Galdieria sulphuraria as observed under a microscope
Scientific classification OOjs UI icon edit-ltr.svg
(unranked): Archaeplastida
Division: Rhodophyta
Class: Cyanidiophyceae
Order: Cyanidiales
Family: Galdieriaceae
Genus: Galdieria
Species:
G. sulphuraria
Binomial name
Galdieria sulphuraria
Merola et al., 1981 [1]

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. sulphurariapH 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]

Contents

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 a source of proteins, especially phycocianin which can be used in diagnostic histochemistry, and as a colorant in cosmetics or food applications. [22] [23] The phycocyanin produced by this species is notable for its thermo and acid resistance, making it suitable for use in the food industry. [24]

Related Research Articles

<span class="mw-page-title-main">Cryptomonad</span> Group of algae and colorless flagellates

The cryptomonads are a group of algae, most of which have plastids. They are traditionally considered a division of algae among phycologists, under the name of Cryptophyta. They are common in freshwater, and also occur in marine and brackish habitats. Each cell is around 10–50 μm in size and flattened in shape, with an anterior groove or pocket. At the edge of the pocket there are typically two slightly unequal flagella. Some may exhibit mixotrophy. They are classified as clade Cryptomonada, which is divided into two classes: heterotrophic Goniomonadea and phototrophic Cryptophyceae. The two groups are united under three shared morphological characteristics: presence of a periplast, ejectisomes with secondary scroll, and mitochondrial cristae with flat tubules. Genetic studies as early as 1994 also supported the hypothesis that Goniomonas was sister to Cryptophyceae. A study in 2018 found strong evidence that the common ancestor of Cryptomonada was an autotrophic protist.

<span class="mw-page-title-main">Unicellular organism</span> Organism that consists of only one cell

A unicellular organism, also known as a single-celled organism, is an organism that consists of a single cell, unlike a multicellular organism that consists of multiple cells. Organisms fall into two general categories: prokaryotic organisms and eukaryotic organisms. Most prokaryotes are unicellular and are classified into bacteria and archaea. Many eukaryotes are multicellular, but some are unicellular such as protozoa, unicellular algae, and unicellular fungi. Unicellular organisms are thought to be the oldest form of life, with early protocells possibly emerging 3.5–4.1 billion years ago.

<span class="mw-page-title-main">Green algae</span> Paraphyletic group of autotrophic eukaryotes in the clade Archaeplastida

The green algae are a group of chlorophyll-containing autotrophic eukaryotes consisting of the phylum Prasinodermophyta and its unnamed sister group that contains the Chlorophyta and Charophyta/Streptophyta. The land plants (Embryophytes) have emerged deep in the Charophyte alga as a sister of the Zygnematophyceae. Since the realization that the Embryophytes emerged within the green algae, some authors are starting to include them. The completed clade that includes both green algae and embryophytes is monophyletic and is referred to as the clade Viridiplantae and as the kingdom Plantae. The green algae include unicellular and colonial flagellates, most with two flagella per cell, as well as various colonial, coccoid (spherical), and filamentous forms, and macroscopic, multicellular seaweeds. There are about 22,000 species of green algae, many of which live most of their lives as single cells, while other species form coenobia (colonies), long filaments, or highly differentiated macroscopic seaweeds.

<span class="mw-page-title-main">Phycocyanin</span> Protein complexes in algae

Phycocyanin is a pigment-protein complex from the light-harvesting phycobiliprotein family, along with allophycocyanin and phycoerythrin. It is an accessory pigment to chlorophyll. All phycobiliproteins are water-soluble, so they cannot exist within the membrane like carotenoids can. Instead, phycobiliproteins aggregate to form clusters that adhere to the membrane called phycobilisomes. Phycocyanin is a characteristic light blue color, absorbing orange and red light, particularly 620 nm, and emits fluorescence at about 650 nm. Allophycocyanin absorbs and emits at longer wavelengths than phycocyanin C or phycocyanin R. Phycocyanins are found in cyanobacteria. Phycobiliproteins have fluorescent properties that are used in immunoassay kits. Phycocyanin is from the Greek phyco meaning “algae” and cyanin is from the English word “cyan", which conventionally means a shade of blue-green and is derived from the Greek “kyanos" which means a somewhat different color: "dark blue". The product phycocyanin, produced by Aphanizomenon flos-aquae and Spirulina, is for example used in the food and beverage industry as the natural coloring agent 'Lina Blue' or 'EXBERRY Shade Blue' and is found in sweets and ice cream. In addition, fluorescence detection of phycocyanin pigments in water samples is a useful method to monitor cyanobacteria biomass.

<span class="mw-page-title-main">Thermoacidophile</span> Microorganisms which live in water with high temperature and high acidity

A thermoacidophile is an extremophilic microorganism that is both thermophilic and acidophilic; i.e., it can grow under conditions of high temperature and low pH. The large majority of thermoacidophiles are archaea or bacteria, though occasional eukaryotic examples have been reported. Thermoacidophiles can be found in hot springs and solfataric environments, within deep sea vents, or in other environments of geothermal activity. They also occur in polluted environments, such as in acid mine drainage.

<span class="mw-page-title-main">Archaeplastida</span> Clade of eukaryotes containing land plants and some algae

The Archaeplastida are a major group of eukaryotes, comprising the photoautotrophic red algae (Rhodophyta), green algae, land plants, and the minor group glaucophytes. It also includes the non-photosynthetic lineage Rhodelphidia, a predatorial (eukaryotrophic) flagellate that is sister to the Rhodophyta, and probably the microscopic picozoans. The Archaeplastida have chloroplasts that are surrounded by two membranes, suggesting that they were acquired directly through a single endosymbiosis event by phagocytosis of a cyanobacterium. All other groups which have chloroplasts, besides the amoeboid genus Paulinella, have chloroplasts surrounded by three or four membranes, suggesting they were acquired secondarily from red or green algae. Unlike red and green algae, glaucophytes have never been involved in secondary endosymbiosis events.

Acidophiles or acidophilic organisms are those that thrive under highly acidic conditions. These organisms can be found in different branches of the tree of life, including Archaea, Bacteria, and Eukarya.

Ostreococcus is a genus of unicellular coccoid or spherically shaped green algae belonging to the class Mamiellophyceae. It includes prominent members of the global picoplankton community, which plays a central role in the oceanic carbon cycle.

<span class="mw-page-title-main">Ochrophyte</span> Phylum of algae

Ochrophytes, also known as heterokontophytes or stramenochromes, are a group of algae. They are the photosynthetic stramenopiles, a group of eukaryotes, organisms with a cell nucleus, characterized by the presence of two unequal flagella, one of which has tripartite hairs called mastigonemes. In particular, they are characterized by photosynthetic organelles or plastids enclosed by four membranes, with membrane-bound compartments called thylakoids organized in piles of three, chlorophyll a and c as their photosynthetic pigments, and additional pigments such as β-carotene and xanthophylls. Ochrophytes are one of the most diverse lineages of eukaryotes, containing ecologically important algae such as brown algae and diatoms. They are classified either as phylum Ochrophyta or Heterokontophyta, or as subphylum Ochrophytina within phylum Gyrista. Their plastids are of red algal origin.

<span class="mw-page-title-main">Red algae</span> Division of plant life

Red algae, or Rhodophyta, make up one of the oldest groups of eukaryotic algae. The Rhodophyta comprises one of the largest phyla of algae, containing over 7,000 recognized species within over 900 genera amidst ongoing taxonomic revisions. The majority of species (6,793) are Florideophyceae, and mostly consist of multicellular, marine algae, including many notable seaweeds. Red algae are abundant in marine habitats. Approximately 5% of red algae species occur in freshwater environments, with greater concentrations in warmer areas. Except for two coastal cave dwelling species in the asexual class Cyanidiophyceae, no terrestrial species exist, which may be due to an evolutionary bottleneck in which the last common ancestor lost about 25% of its core genes and much of its evolutionary plasticity.

<span class="mw-page-title-main">Eukaryote</span> Domain of life whose cells have nuclei

The eukaryotes constitute the domain of Eukarya or Eukaryota, organisms whose cells have a membrane-bound nucleus. All animals, plants, fungi, and many unicellular organisms are eukaryotes. They constitute a major group of life forms alongside the two groups of prokaryotes: the Bacteria and the Archaea. Eukaryotes represent a small minority of the number of organisms, but given their generally much larger size, their collective global biomass is much larger than that of prokaryotes.

<i>Cyanidioschyzon</i> Species of alga

Cyanidioschyzon merolae is a small (2μm), club-shaped, unicellular haploid red alga adapted to high sulfur acidic hot spring environments. The cellular architecture of C. merolae is extremely simple, containing only a single chloroplast and a single mitochondrion and lacking a vacuole and cell wall. In addition, the cellular and organelle divisions can be synchronized. For these reasons, C. merolae is considered an excellent model system for study of cellular and organelle division processes, as well as biochemistry and structural biology. The organism's genome was the first full algal genome to be sequenced in 2004; its plastid was sequenced in 2000 and 2003, and its mitochondrion in 1998. The organism has been considered the simplest of eukaryotic cells for its minimalist cellular organization.

<i>Ostreococcus tauri</i> Species of alga

Ostreococcus tauri is a unicellular species of marine green alga about 0.8 micrometres (μm) in diameter, the smallest free-living (non-symbiotic) eukaryote yet described. It has a very simple ultrastructure, and a compact genome.

<span class="mw-page-title-main">Cyanidiophyceae</span> Class of algae

Cyanidiophyceae is a class of unicellular red algae within subdivision Cyanidiophytina, and contain a single plastid, one to three mitochondria, a nucleus, a vacuole, and floridean starch. Pyrenoids are absent. Most are extremophiles inhabiting acid hot springs. They originated in extreme environments with high themperatures and low pH, which allowed them to occupy ecological niches without any competition. While still found in extreme environmnets, they have also adapted to live along streams, in fissures in rock walls and in soil, but usually prefer relatively high temperatures. They have never been found in basic freshwater or seawater habitats. The main photosynthetic pigment is C-phycocyanin. Reproduction is asexual by binary fission or formation of endospores. The group, consisting of a single order (Cyanidiales), split off from the other red algae more than a billion years ago. Three families, four genera, and nine species are known, but the total number of species is probably higher. They are primarily photoautotrophic, but heterotrophic and mixotrophic growth also occurs. After the first massive gene loss in the common ancestor of all red algae, where ca. 25% of the genes were lost, a second gene loss occurred in the ancestor of Cyanidiophyceae, where additional 18% of the genes were lost. Since then, some gene gains and minor gene losses have taken place independently in the Cyanidiaceae and Galdieriaceae, leading to genetic diversification between the two groups, with Galdieriaceae occupying more diverse and varied niches in extreme environments than Cyanidiaceae.

Vitrella brassicaformis (CCMP3155) is a unicellular alga belonging to the eukaryotic supergroup Alveolata. V. brassicaformis and its closest known relative, Chromera velia, are the only two currently described members of the phylum Chromerida, which in turn constitutes part of the taxonomically unranked group Colpodellida. Chromerida is phylogenetically closely related to the phylum Apicomplexa, which includes Plasmodium, the agent of malaria. Notably, both V. brassicaformis and C. velia are photosynthetic, each containing a complex secondary plastid. This characteristic defined the discovery of these so-called 'chromerids,' as their photosynthetic capacity positioned them to shed light upon the evolution of Apicomplexa's non-photosynthetic parasitism. Both genera lack chlorophyll b or c; these absences link the two taxonomically, as algae bearing only chlorophyll a are rare amid the biodiversity of life. Despite their similarities, V. brassicaformis differs significantly from C. velia in morphology, lifecycle, and accessory photosynthetic pigmentation. V. brassicaformis has a green color, with a complex lifecycle involving multiple pathways and a range of sizes and morphologies, while Chromera has a brown color and cycles through a simpler process from generation to generation. The color differences are due to differences in accessory pigments.

<span class="mw-page-title-main">Picozoa</span> Phylum of marine unicellular heterotrophic eukaryotes

Picozoa, Picobiliphyta, Picobiliphytes, or Biliphytes are protists of a phylum of marine unicellular heterotrophic eukaryotes with a size of less than about 3 micrometers. They were formerly treated as eukaryotic algae and the smallest member of photosynthetic picoplankton before it was discovered they do not perform photosynthesis. The first species identified therein is Picomonas judraskeda. They probably belong in the Archaeplastida as sister of the Rhodophyta.

Picrophilus torridus is a species of Archaea described in 1996. Picrophilus torridus was found in soil near a hot spring in Hokkaido, Japan. The pH of the soil was less than 0.5. P. torridus also has one of the smallest genomes found among organisms that are free-living and are non-parasitic and a high coding density, meaning that the majority of its genes are coding regions and provide instructions for building proteins. The current research suggests the two hostile conditions favored by P. torridus have exerted selective pressure towards having a small and compact genome, which is less likely to be damaged by the harsh environment.

<span class="mw-page-title-main">Floridean starch</span> Type of storage glucan

Floridean starch is a type of a storage glucan found in glaucophytes and in red algae, in which it is usually the primary sink for fixed carbon from photosynthesis. It is found in grains or granules in the cell's cytoplasm and is composed of an α-linked glucose polymer with a degree of branching intermediate between amylopectin and glycogen, though more similar to the former. The polymers that make up floridean starch are sometimes referred to as "semi-amylopectin".

Galdieria is a genus of red algae belonging to the order Galdieriales; family Galdieriaceae. It was created by an Italian botanist Aldo Merola in 1981 for the identification from the species of Cyanidium.

<i>Galdieria partita</i> Species of red algae

Galdieria partita is a species of extremophilic red algae that lives in acidic hot springs. It is the only unicellular species of red algae known to reproduce sexually. It was discovered in 1894 by Josephine Elizabeth Tilden from Yellowstone National Park in the western United States. Originally described as a specides of green algae, Chroococcus varium, its scientific name and taxonomic position were revised several times. In 1959, Mary Belle Allen produced the pure culture which has been distributed as the "Allen strain".

References

  1. 1 2 3 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. 1 2 Guiry, M.D.; Guiry, G.M. "Galdieria sulphuraria". AlgaeBase . World-wide electronic publication, National University of Ireland, Galway.
  3. 1 2 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. 1 2 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. 1 2 3 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.
  22. Abiusi, Fabian; Moñino Fernández, Pedro; Canziani, Stefano; Janssen, Marcel; Wijffels, René H.; Barbosa, Maria (2022-01-01). "Mixotrophic cultivation of Galdieria sulphuraria for C-phycocyanin and protein production". Algal Research. 61: 102603. doi:10.1016/j.algal.2021.102603. hdl: 11250/2978302 . ISSN   2211-9264.
  23. Pagels, Fernando; Guedes, A. Catarina; Amaro, Helena M.; Kijjoa, Anake; Vasconcelos, Vitor (2019-05-01). "Phycobiliproteins from cyanobacteria: Chemistry and biotechnological applications". Biotechnology Advances. 37 (3): 422–443. doi:10.1016/j.biotechadv.2019.02.010. ISSN   0734-9750.
  24. Wan, Minxi; Zhao, Haoyu; Guo, Jiacai; Yan, Lulu; Zhang, Daojing; Bai, Wenmin; Li, Yuanguang (2021-10-01). "Comparison of C-phycocyanin from extremophilic Galdieria sulphuraria and Spirulina platensis on stability and antioxidant capacity". Algal Research. 58: 102391. doi:10.1016/j.algal.2021.102391. ISSN   2211-9264.