Summary of the main features characterizing the most abundant pigments in bird feathers.
Some seabirds or coastal birds such as flamingos or pelicans display elegant pink or reddish colours. These colours are due to pigments that birds cannot synthesize de novo. Thus, this coloration is mainly originated from carotenoids ingested trough carotenoid rich food sources like microalgae (Dunaliella) or small shrimps (Artemia), which are microorganisms inhabiting the salty environments where the mentioned birds live. New advances in this field of knowledge have revealed that extreme microorganisms belonging to the haloarchaea group (Archaea Domain) may contribute significantly to the characteristic pink- red colour of flamingos’ feathers for instance. Alive haloarchaea cells have been found on the surface of the feathers. Besides, the major carotenoid produced by haloarchaea (bacterioruberin) has also been identify within the feathers structure. This work summarizes the main contributions recently reported about this topic as well as general aspects regarding bacterioruberin as a powerful colour carotenoid. Discussions about potential role of these microorganisms in the life of seaside birds are also included.
- bird coloration
- natural pigments
Coloration is one of the most conspicuous traits that varies among organisms. In the case of animals, colour is mainly due to: (i) the presence of pigments (carotenoids, melanin, turacoverdin, biliverdin, protoporphyrin, etc); (ii) light phenomena such as reflection/emission from animal structures (skin, feathers, etc.); (iii) the presence of microscopic structure in scales, bristles, or feathers, which give them brilliant iridescent colours (commonly named “structural colours”) ; and (iv) general aspects related to genetics . Due to these reasons, animals show different colours, which can slightly vary even between individuals belonging to the same species. Animal colorations are strongly linked to different biological roles: camouflage, sexual, social, and interspecific signalling, physical protection (against UV radiation for instance), and sexual dimorphism [3, 4, 5, 6].
In the case of the birds, feathers play a key role in general coloration. Those that are red orange show these colours thanks to the presence of different carotenoids within their structures. Carotenoids are natural pigments widely spread in nature: chloroplasts and chromoplasts of plants, bacteria, archaea, microalgae, fungi and even phytoplankton [7, 8, 9]. All the mentioned organisms can synthesize carotenoids, but animals in general are not able to produce them
There are over 600 known carotenoids classified into two classes: xanthophylls (which contain oxygen) and carotenes (which are hydrocarbons without oxygen). Thanks to their chemical structure, they absorb wavelengths ranging from 400–550 nanometres (violet to green light) . Consequently, these pigments are deeply coloured yellow, orange or red. Some carotenoids have vitamin A activity (they can be converted into retinol) and most of them can also act as antioxidants. Recently, it has been stated that cytochrome P450 enzymes are also involved in red carotenoid coloration .
Red coloured birds inhabiting salted environments such as salt marshes, seaside ecosystems, salted lagoons etc. may often acquire carotenoids by ingesting small organisms or even microorganisms like yeast and algae. Thus, flamingos (
The nature of the colour shown by red-pink feathers is one of the aspects strongly discussed during the last few years. Many works have demonstrated that the colour is due to the carotenoids obtained through the diet, whilst other studies suggested that other external factors like microorganisms or light phenomena could contribute to the final red-orange-pink phenotype. This chapter summarizes recent knowledge about the presence of alive microorganisms belonging to the Archaea domain on the surface of red-pink feathers thus may contributing to their colour. General aspects related to the carotenoids produced by haloarchaea inhabiting feathers of coastal birds are also discussed.
2. The colour of bird feathers
Bird feathers have been the aim of several works during the last two centuries. Thus, the first reports on bird plumage listed in databases like PUBMED, Web of Science or Scopus analysed aspects focused on the muscles in charge of the feathers movement  or their growth . Other aspects of bird feathers related to biological roles like sexual selection, colonization strategies or signalling have also been extensively explored [19, 20, 21, 22, 23]. These aspects are intricately connected to the coloration of avian plumage.
The first detailed studies about the colour of bird feathers were published in indexed scientific journals in the middle fifties last century. Since then, around 500 manuscripts have been reported on this subject (Figure 1). It is worthy to note that the number of studies about the colouration of plumage significantly increased at the beginning of XXI century (Figure 1). However, the number of publications focused on the presence of carotenoids in bird feathers is lower compared to those related to other issues affecting the phenotype of birds (Figure 1). Bird coloration (mainly in feathers) is one of the most studied topics to elucidate the role of natural and sexual selection in the evolution of phenotypic diversity. Thus, the variety of vibrant plumage colours has evolved as a direct result of social and environmental pressures.
The colour of plumage and other structures in animals and plants is due to the presence of pigments (pigment-based coloration) or the presence of microscopically structured surfaces fine enough to interfere with visible light (structural coloration) . Iridescence for instance, is one of the better-known examples of it . In some cases, feather colours are the result of a combination of both [26, 27].
Table 1 summarizes the most representative pigments already identified as part of the colour of bird plumage. The most abundant are melanin and carotenoids [28, 42]. On the one hand, melanin-based coloration switches from brown to black due to the presence of phaeomelanin or eumelanin, respectively, or the number and distribution of the melanosomes [29, 30]. On the other hand, carotenoids-based colorations vary from yellow to red as previously mentioned.
|Eumelanin||Grey/Black||[28, 29, 30, 31]|
|Pheomelanin||Brown||[28, 29, 31, 32]|
|Zeaxanthin||Yellow||[2, 33, 34]|
|Lutein||Bright Yellow||[2, 33, 34, 35]|
|Canthaxanthin||Orange Red||[2, 33, 34, 35]|
|Astaxanthin||Red||[2, 34, 35, 36]|
|Rhodoxanthin||Purple-red||[34, 37, 38]|
|Coproporphyrin III||Red Brown|||
The genetics of coloration in birds remains poorly described. However, it is extensively accepted that its expression is phenotypically plastic with a high sensitivity to variation in environmental conditions. Therefore, the melanin-based colour should be considered the key system to understand the molecular basis of phenotypic variations . Some other pigments are only present in some species. This is the case of psittacofulvins, which are found just in a few species of parrots (
Archaea, one of the three Domains of life, make up a significant fraction of the microbial biomass on Earth . It was thought that Archaea microbes were restricted to extreme environments, such as those with elevated temperatures, low or high pH, high salinity, or strict anoxia . However, environmental sampling analysis based on rRNA sequences has revealed that archaea are widespread in “normal” ecosystems, including soils, oceans, marshlands, human colon, human oral cavity and even in human skin. They are particularly numerous in the oceans; thus, archaea in plankton may constitute one of the most abundant groups of organisms on the planet. From a metabolic point of view, they have evolved a variety of energy metabolisms using organic and/or inorganic electron donors and acceptors, playing important roles in the Earth’s global geochemical cycles .
Salty environments are dominated by organisms commonly named “halophiles” (it comes from the Greek word for “salt-loving”). They are usually classified into three groups according to their NaCl requirements: slight halophiles (2–5% or 0.34–0.85 M), moderate halophiles (5–20% or 0.85–3.4 M) and extreme halophiles (20–30% or 3.4–5.1 M) .
Halophilic archaea, also called Haloarchaea, are extreme or moderated halophilic species inhabiting neutral saline environments such as salt lakes, marine salterns, marshes, saltern crystallizer ponds or genuine environments like the Dead Sea [51, 52]. In those natural ecosystems, salt concentrations are around 1.5–4 M, which corresponds to 9–30% of salts (w/v). NaCl is the predominant salt and ionic proportions are like those dissolved salts in seawater.
These halophilic ecosystems harbour a large diversity of microorganisms of all three domains: small eukaryotes such the shrimp
4. Haloarchaea and their relation to avian plumage colour: the case of marine birds
Studies in the early nineties of the last century demonstrated that the carotenoids of the feathers were derived from the diet and deposited within tissues selectively  being the liver one of the most important organs involved in the conversion of carotenoids uptaken . Some years before, other studies focused on seaside birds as flamingos stated that the major carotenoids in blood and feathers were canthaxanthin and a rare β-carotene derivative (4-keto-α-carotene) [55, 56]. Limitations on chemical and analytical techniques have contribute to the poor knowledge about carotenoids in birds up to nowadays. Fortunately, new advances in spectrometry and HPLC have made possible a significant improvement in this field of knowledge [41, 57]. Thus, during the last 15 years, several research groups worldwide have characterised the nature (and even the concentrations) of carotenoids in blood and feathers, mainly in finches [58, 59] and parrots [44, 60]. All the reported results show that the most important carotenoids contributing to the red-orange-pink colours in feathers are: canthaxanthin, astaxanthin, zeaxanthin and carotene (including its derivatives). In the case of seaside birds, it has been stated that the main rich carotenoids sources are the small shrimps and algae co-inhabiting the salty environments (
Recent contributions in this field have revealed that there are other important factors contributing to the red-orange-pink colour of the feathers. Between them, it is important to highlight the following: (i) genetics ; (ii) variation in carotenoid-protein interactions in bird feathers structures, which produces novel plumage coloration  and (iii) the presence of alive red-orange microorganisms on the surface of the feathers . This last factor has recently been reported from flamingos growing up in captivity: viable, red-coloured archaeal strains belonging to the genera
This carotenoid is involved in several biological roles in haloarchaea: it protects the cells against the damage produced by high intensities of sun radiation, it provides aid in photoreactivation  and it promotes membranes stability [8, 65]. Characterisation of pure bacterioruberin samples revealed that it is more powerful than carotene as antioxidant compound [67, 68]. Due to these facts, bacterioruberin could be used in biotechnology and biomedicine for different purposes [8, 69].
Consequently, haloarchaea in general and their pigments in particular, may contribute to the orange-red colour of the feathers in two ways: (i) pink-red haloarchaea cells on the surface contribute to the pink-red phenotype in flamingos’ feathers and (ii) haloarchaeal cells are part of the marine birds’ diet (at least flamingos), consequently their carotenoids (mainly bacterioruberin) are ingested, metabolised and further assimilated.
New advances in the knowledge of animal pigmentation state that not only the pigments (carotenoids, melanin, etc.), but also the microstructure of the feathers as well as external factors, contribute to the final phenotype in terms of coloration. Related to birds, and particularly to seaside birds, it was thought that microalgae and small shrimps were the major sources of carotenoids so far. Nevertheless, recent results revealed that other small microbes such as haloarchaea could contribute significantly to the red-orange colours showed by birds like flamingos. In that sense, bacterioruberin becomes a new pigment to be considered to explain animal colours in marine environments. The potential influence of haloarchaea as an environmental factor determining avian plumage coloration or even protecting the microstructures of feathers against UV radiation must be investigated in further studies. Although bacterioruberin has been very well described, only few studies about its biological implications are available at the time of writing this review. Thus, more efforts must be done to explain basic aspects related to bacterioruberin metabolism and its effects on animal health and animal phenotypes. On the other hand, associations between different haloarchaeal-bird species as well as changes in these associations promoted by environmental conditions or anthropogenic actions are worthy to be analysed into detail. Hypothesis based on potential symbiotic relationship between haloarchaea and seaside birds remains unexplored.
This work was funded by research grant from the University of Alicante (VIGROB-309). The authors would like to thank Francisco Grimalt Salvá and José Antonio Abellán for their helpful discussions about the color of the feathers in genera of the
Conflict of interest
The authors declare no conflict of interest.
Prum RO, Torres R. Structural colouration of avian skin: convergent evolution of coherently scattering dermal collagen arrays. J Exp Biol 2003;206: 2409-2429.
Lopes RJ, Johnson JD, Toomey MB, Ferreira MS, Araujo PM, Melo-Ferreira J, Andersson L, Hill GE, Corbo JC, Carneiro M. Genetic basis for red coloration in birds. Curr Biol 2016;26:1427-1434.
Finger E, Burkhardt D. Biological aspects of bird colouration and avian colour vision including ultraviolet range. Vision Research 1994;34:1509-1514.
Stuart-Fox D, Moussalli A. Camouflage, communication and thermoregulation: lessons from colour changing organisms. Philos Trans R Soc Lond B Biol Sci 2009;364:463-470.
Freeman HD, Valuska AJ, Taylor RR, Ferrie GM, Grand AP, Leighty KA. Plumage variation and social partner choice in the greater flamingo ( Phoenicopterus roseus). Zoo Biology 2016;35:409-414.
Duarte RC, Flores AAV, Stevens M. Camouflage through colour change: mechanisms, adaptive value and ecological significance. Philos Trans R Soc Lond B Biol Sci. Series B, Biological Sciences 2017;372:20160342.
Rodríguez-Ortiz R, Michielse C, Rep M, Limón MC, Avalos J. Genetic basis of carotenoid overproduction in Fusarium oxysporum. Fungal Genet Biol 2012;49:684-696.
Rodrigo-Baños M, Garbayo I, Vílchez C, Bonete MJ, Martínez-Espinosa RM. Carotenoids from Haloarchaea and their potential in Biotechnology. Mar Drugs 2015;13:5508-5532.
Huang JJ, Lin S, Xu W, Cheung PCK. Occurrence and biosynthesis of carotenoids in phytoplankton. Biotechnol Adv 2017;35:597-618.
Altincicek B, Kovacs JL, Gerardo NM. Horizontally transferred fungal carotenoid genes in the two-spotted spider mite Tetranychus urticae. Biology Letters 2011;8:253-257.
Nagao A. Oxidative conversion of carotenoids to retinoids and other products. J Nutr 2004;134:237S–240S.
Harrison EH, Curley RW. Carotenoids and retinoids: nomenclature, chemistry, and analysis. Sub-cellular Biochemistry 2016;81:1-19.
Mundy NI, Stapley J, Bennison C, Tucker R, Twyman H, Kim KW, Burke T, Birkhead TR, Andersson S, Slate J. Red carotenoid coloration in the zebra finch is controlled by a cytochrome P450 gene cluster. Curr Biol 2016;26:1435-1440.
Oren A. A hundred years of Dunaliellaresearch: 1905-2005. Saline Systems 2005;1:2.
Hill GE, Montgomerie R, Inouye CY, Dale J. Influence of dietary carotenoids on plasma and plumage colour in the house finch: intra- and intersexual variation. Functional Ecology 1994;8:343-350.
Toews DP, Hofmeister NR, Taylor SA. The Evolution and Genetics of Carotenoid Processing in Animals. Trends Genet 2017;33:171-182.
Langley JN. On the sympathetic system of birds and on the muscles which move the feathers. J Physiol 1903;30:221-252.
Danforth CH. The effect of foreign skin on feather pattern in the common fowl ( Gallus domesticus). Wilhelm Roux' Archiv Fur Entwicklungsmechanik Der Organismen 1929;116:242-252.
Dunn PO, Armenta JK, Whittingham LA. Natural and sexual selection act on different axes of variation in avian plumage color. Scientific Advances 2015;1:e1400155.
Doutrelant C, Paquet M, Renoult JP, Grégoire A, Crochet PA, Covas R. Worldwide patterns of bird colouration on islands. Ecol Lett 2016;19:537-545.
Marques CI, Batalha HR, Cardoso GC. Signalling with a cryptic trait: the regularity of barred plumage in common waxbills. R Soc Open Sci 2016; 3:160195.
Shultz AJ, Burns KJ. The role of sexual and natural selection in shaping patterns of sexual dichromatism in the largest family of songbirds (Aves: Thraupidae). Evolution 2017;71:1061-1074.
Galván I, Jorge A, Pacheco C, Spencer D, Halley DJ, Itty C, Kornan J, Nielsen JT, Ollila T, Sein G, Stój M, Negro JJ. Solar and terrestrial radiations explain continental-scale variation in bird pigmentation. Oecologia 2018;188:683-693.
Eliason CM, Maia R, Shawkey MD. Modular color evolution facilitated by a complex nanostructure in birds. Evolution 2015;69:357-367.
Kinoshita S, Yoshioka S. Structural colours in nature: the role of regularity and irregularity in the structure. Chem Phys Chem 2005;6:1442-1459.
Martínez-Espinosa RM. Influencia del color estructural en el color amarillo pigmentario de las plumas. Revista Ornitológica Práctica 2010;43:64-67.
LaFountain A, Prum RO, Frank HA. Diversity, physiology, and evolution of avian plumage carotenoids and the role of carotenoid-protein interactions in plumage color appearance. Arch Biochem Biophys 2015;572:201-212.
Galván I, Solano F. Bird Integumentary melanins: biosynthesis, forms, function and evolution. Int J Mol Sci 2016;17:520.
Roulin A, Almasi B, Meichtry-Stier KS. Jenni L. Eumelanin- and pheomelanin-based colour advertise resistance to oxidative stress in opposite ways. J Evol Biol 2011;24: 2241-2247.
Edwards NP, van Veelen A, Anné J, Manning PL, Bergmann U, Sellers WI, Egerton VM, Sokaras D, Alonso-Mori R, Wakamatsu K, Ito S, Wogelius RA. Elemental characterisation of melanin in feathers via synchrotron X-ray imaging and absorption spectroscopy. Sci Rep 2016;6: 34002.
Zduniak P, Surmacki A, Erciyas-Yavuz K, Chudzińska M, Barałkiewicz D. Are there different requirements for trace elements in eumelanin- and pheomelanin-based color production? A case study of two passerine species. Comp Biochem Physiol A Mol Integr Physiol 2014;175: 96-101.
Galván I, Jorge A, Solano F, Wakamatsu K. Vibrational characterization of pheomelanin and trichochrome F by Raman spectroscopy. Spectrochim Acta A Mol Biomol Spectrosc 2013;110: 55-59.
Sparrow KL, Donkor KK, Flood NJ, Marra PP, Pillar AG, Reudink MW. Conditions on the Mexican moulting grounds influence feather colour and carotenoids in Bullock’s orioles ( Icterus bullockii). Ecol Evol 2017;7:2643-2651.
Prum RO, LaFountain AM, Berro J, Stoddard MC, Frank HA. Molecular diversity, metabolic transformation, and evolution of carotenoid feather pigments in cotingas (Aves: Cotingidae). J Comp Physiol B 2012;182: 095-1116.
Hudon J, Wiebe KL, Pini E, Stradi R. Plumage pigment differences underlying the yellow-red differentiation in the Northern Flicker ( Colaptes auratus). Comp Biochem Physiol B Biochem Mol Biol 2015;183:1-10.
García-de Blas E, Mateo R, Guzmán Bernardo FJ, Rodríguez Martín-Doimeadios RC, Alonso-Álvarez C. Astaxanthin and papilioerythrinone in the skin of birds: a chromatic convergence of two metabolic routes with different precursors? Naturwissenschaften 2014;101: 407-416.
Berg CJ, LaFountain AM, Prum RO, Frank HA, Tauber MJ. Vibrational and electronic spectroscopy of the retro-carotenoid rhodoxanthin in avian plumage, solid-state films and solution. Arch Biochem Biophys 2013;539: 142-155.
Hudon J, Anciães M, Bertacche V, Stradi R. Plumage carotenoids of the Pin-tailed Manakin ( Ilicura militaris): evidence for the endogenous production of rhodoxanthin from a colour variant. Comp Biochem Physiol B Biochem Mol Biol 2007;147: 402-411.
Gill W, Frank B. Feathers. In F. B. Gill (Ed), Ornithology. Part II, chapter 2006;4 p. 97, New York: W.H. Freeman and Company.
Negro JJ, Bortolotti GR, Mateo R, García IM. Porphyrins and pheomelanins contribute to the reddish juvenal plumage of black-shouldered kites. Comp Biochem Physiol B Biochem Mol Biol 2009;153: 296-299.
Toral GM, Figuerola J, Negro JJ. Multiple ways to become red: pigment identification in red feathers using spectrometry. Comp Biochem Physiol B Biochem Mol Biol 2008;150: 147-152.
Dey CJ, Valcu M, Kempenaers B, Dale J. Carotenoid-based bill coloration functions as a social, not sexual, signal in songbirds (Aves: Passeriformes). J Evol Biol 2015;28:250-258.
Roulin A, Ducrest AL. Genetics of colouration in birds. Semin Cell Dev Biol 2013;24: 594-608.
McGraw KJ, Nogare MC. Carotenoid pigments and the selectivity of psittacofulvin-based coloration systems in parrots. Comp Biochem Physiol B Biochem Mol Biol 2004;138: 229-233.
Thomas DB, McGoverin CM, McGraw KJ, James HF, Madden O. Vibrational spectroscopic analyses of unique yellow feather pigments (spheniscins) in penguins. J R Soc Interface 2013;10: 20121065.
Tinbergen J, Wilts BD, Stavenga DG. Spectral tuning of Amazon parrot feather coloration by psittacofulvin pigments and spongy structures. J Exp Biol 2013;216: 4358-4364.
Woese CR, Kandler O, Wheelis M. Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eukarya. Proc Natl Acad Sci U S A 1990;87: 4576-4579.
Valentine DL. Adaptations to energy stress dictate the ecology and evolution of the Archaea. Nat Rev Microbiol 2007;5: 316-323.
Offre P, Spang A, Schleper C. Archaea in biogeochemical cycles. Annu Rev Microbiol 2013;67: 437-457.
Larsen H. Halophilism. In: Gunsalus, I.C. and Stanier, R.Y. (eds.). The bacteria, 1962;pp 297-342. Editorial: Academic Press, New York.
Grant WD, Kamekura M, Mc Genity TJ, Ventosa A. Class III. Halobacteria class. nov. In, D. R. Boone, R. W. Castenholz, R. & G. M. Garrity (Eds), Bergey’s manual of systematic bacteriology: Vol. 1. 2nd Ed., 2001;pp. 294-334. New York: Springer Verlag.
Oren A. Halophilic microorganisms and their environments. In: J. Seckbach (ed). Cellular Origin, Life in Extreme Habitats and Astrobiology, 2002;pp 527. Editorial: Kluwer Academic Publishers.
Brush AH. Metabolism of carotenoid pigments in birds. FASEB J 1990;4: 2969-2977.
Del Val E, Senar JC, Garrido-Fernández J, Jarén M, Borràs A, Cabrera J, Negro JJ. The liver but not the skin is the site for conversion of a red carotenoid in a passerine bird. Naturwissenschaften 2009;96: 797-801.
Fox DL, Hopkins TS. Comparative metabolic fractionation of carotenoids in three flamingo species. Comp Biochem Physiol 1966;17: 841-856.
Fox DL, Smith VE, Wolfson AA. Carotenoid selectivity in blood and feathers of lesser (African), Chilean and greater (European) flamingos. Comp Biochem Physiol 1967;23: 225-232.
García-de Blas E, Mateo R, Viñuela J, Alonso-Álvarez C. Identification of carotenoid pigments and their fatty acid esters in an avian integument combining HPLC-DAD and LC-MS analyses. J Chromatogr B Analyt Technol Biomed Life Sci 2011;879: 341-348.
McGraw KJ, Hill GE, Stradi R, Parker RS. The influence of carotenoid acquisition and utilization on the maintenance of species-typical plumage pigmentation in male American goldfinches ( Carduelis tristis) and northern cardinals (Cardinalis cardinalis). Physiol Biochem Zool 2001;74: 843-852.
McGraw KJ, Schuetz JG. The evolution of carotenoid coloration in estrildid finches: a biochemical analysis. Comp Biochem Physiol B Biochem Mol Biol 2004;139: 45-51.
McGraw KJ, Nogare MC. Distribution of unique red feather pigments in parrots. Biol Lett 2005;1: 38-43.
Masero JA. Why don’t red knots Calidris canutusfeed extensively on the crustacean Artemia? Bird Study 2002;49: 304-306.
Mendes-Pinto MM, LaFountain AM, Stoddard MC, Prum RO, Frank HA, Robert B. Variation in carotenoid-protein interaction in bird feathers produces novel plumage coloration. J R Soc Interf 2012;9: 3338-3350.
Yim KJ, Kwon J, Cha IT, Oh KS, Song HS, Lee HW, Rhee JK, Song EJ, Rho JR, Seo ML, Choi JS, Choi HJ, Lee SJ, Nam YD, Roh SW. Occurrence of viable, red-pigmented haloarchaea in the plumage of captive flamingoes. Sci Rep 2015;5: 16425.
Montero-Lobato Z, Ramos-Merchante A, Fuentes JL, Sayago A, Fernández-Recamales Á, Martínez-Espinosa RM, Vega JM, Vílchez C, Garbayo I. Optimization of growth and carotenoid production by Haloferax mediterraneiusing response surface methodology. Mar Drugs 2018;9; 16(10). pii: E372.
Torregrosa-Crespo J, Montero Z, Fuentes JL, Reig García-Galbis M, Garbayo I, Vílchez C, Martínez-Espinosa RM. Exploring the valuable carotenoids for the large-scale production by marine microorganisms. Mar Drugs 2018;16(6). pii: E203.
Shahmohammadi HR, Asgarani E, Terato H, Saito T, Ohyama Y, Gekko K, Yamamoto O, Ide H. Protective roles of bacterioruberin and intracellular KCl in the resistance of Halobacterium salinariumagainst DNA-damaging agents. J Radiat Res 1998;39: 251-262.
Saito T, Miyabe Y, Ide H, Yamamoto O. Hydroxyl radical scavenging ability of bacterioruberin. Radiat Phys Chem 1997;50: 267-269.
Kottemann M, Kish A, Iloanusi C, Bjork S, DiRuggiero J. Physiological responses of the halophilic archaeon Halobacteriumsp. strain NRC1 to desiccation and gamma irradiation. Extremophiles 2005;9: 219-227.
Hou J, Cui HL. In Vitro Antioxidant, Antihemolytic, and Anticancer Activity of the Carotenoids from Halophilic Archaea. Curr Microbiol 2017;75: 266-271.