Map of the global distribution of flamingo habitats and haloarchaeal isolation sites.: Flamingo habitats are indicated by a pink color and haloarchaeal sites are shown by blue triangles. The map was created using Adobe Illustrator software (Adobe Systems, Mountain View, CA, USA). The sources of haloarchaeal isolation sites can be found in Supplementary Information. The information of flamingo habitats was obtained from Wikimedia Commons (http://commons.wikimedia.org/wiki/File%3AFlamingo_range.png).

Map of the global distribution of flamingo habitats and haloarchaeal isolation sites.: Flamingo habitats are indicated by a pink color and haloarchaeal sites are shown by blue triangles. The map was created using Adobe Illustrator software (Adobe Systems, Mountain View, CA, USA). The sources of haloarchaeal isolation sites can be found in Supplementary Information. The information of flamingo habitats was obtained from Wikimedia Commons (http://commons.wikimedia.org/wiki/File%3AFlamingo_range.png).

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Flamingoes (Phoenicopterus spp.) whose plumage displays elegant colors, inhabit warm regions close to the ocean throughout the world. The pink or reddish color of their plumage originates from carotenoids ingested from carotenoid-abundant food sources, since flamingoes are unable to synthesize these compounds de novo. In this study, viable red-colo...

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... The source of the beautiful, brilliant colors of bird feathers can be pigmented or structural. Pigment colors; include melanin (D'Alba et al., 2014;Galván and Solano, 2016), carotenoids Thomas et al., 2014;Thomas and James, 2005;Shawkey and Hill, 2005;McGraw and Toomey, 2010;Yim et al., 2015), porphyrins (With, 1978), psittacofarvin (Tin-bergen et al., 2013), and spheniscin (Thomas et al., 2012), and structural colors; include thin-film interference of cortical β-keratin (Nakamura et al., 2008;Eliason and Shawkey, 2010;Stavenga, 2014;Okazaki, 2019), a spongy layer bellow the cortex (Shawkey et al., 2009;Yin et al., 2012;Saranathan et al., 2012;Prum et al., 2009;Okazaki, 2020a;Stavenga et al., 2011), and the lattice structure of melanin granules (Yoshioka and Kinoshita, 2002;Zi et al., 2003;Dakin and Montgomerie, 2013;Medina et al., 2015). When either the left-or right-handed CPL was irradiated on the surface of dove and mallard feathers, the structural color reflected the left-or right-handed CPL opposite to the direction of irradiated light. ...
... Bacterioruberin is also currently used to encapsulate drugs, allowing its safe administration and stability capable of resisting the human stomach's harsh environment [18]. Also, the haloarchaeal carotenoid-based pigments may contribute to the distinctive colours of flamingo's feathers coloration either by colonization or accumulation in the food chain (small salt crustaceans) and are one of the environmental factors behind their plumage coloration [19]. ...
Article
Haloarchaea are mostly components of the microbial biomass of saline aquatic environments, where they can be a dietary source of heterotrophic metazoans or contribute to flamingo’s plumage coloration. The diversity of secondary metabolites (SMs) produced by haloarchaea, which might play multiple ecological roles and have diverse biotechnological applications has been largely understudied. Herein, 67 haloarchaeal complete genomes were analyzed and 182 SMs biosynthetic gene clusters (BGCs) identified that encode the production of terpenes (including carotenoids), RiPPs and siderophores. Terpene BGCs were further analysed and it was concluded that all haloarchaea might produce squalene and bacterioruberin, which one a strong antioxidant. Most of them have other carotenoid BGCs that include a putative β-carotene ketolase that was not characterized so far in haloarchaea, but may be involved with canthaxanthin's biosynthesis. The production of bacterioruberin by Haloferax mediterranei ATCC 33500 was found to be not related to its antimicrobial activity.
... 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 [2]; (ii) variation in carotenoidprotein interactions in bird feathers structures, which produces novel plumage coloration [63] and (iii) the presence of alive red-orange microorganisms on the surface of the feathers [64]. This last factor has recently been reported from flamingos growing up in captivity: viable, red-coloured archaeal strains belonging to the genera Halococcus and Halogeometricum were isolated from the surface of the plumage [64]. ...
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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.
... Information regarding the community-based genetic and functional traits of archaea in animal habitats is scarce. We have previously reported occurrences of diverse members of extremely halophilic archaea (haloarchaea) in avian plumage [13], as well as in food samples such as salt-fermented seafood [14] and solar salts [15,16]. In the human gut where the microbial entities thrive more abundantly than in other parts of the human body, the archaeome consisted mostly of methane-producing archaea (methanogens), of which, members belonging to the orders Methanobacteriales (including Methanobrevibacter smithii and Methanosphaera stadtmanae) and Methanomassiliicoccales (including Methanomethylophilaceae) are predominant [17]. ...
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Background: Archaea are one of the least-studied members of the gut-dwelling autochthonous microbiota. Few studies have reported the dominance of methanogens in the archaeal microbiome (archaeome) of the human gut, although limited information regarding the diversity and abundance of other archaeal phylotypes is available. Results: We surveyed the archaeome of faecal samples collected from 897 East Asian subjects living in South Korea. In total, 42.47% faecal samples were positive for archaeal colonisation; these were subsequently subjected to archaeal 16S rRNA gene deep sequencing and real-time quantitative polymerase chain reaction-based abundance estimation. The mean archaeal relative abundance was 10.24 ± 4.58% of the total bacterial and archaeal abundance. We observed extensive colonisation of haloarchaea (95.54%) in the archaea-positive faecal samples, with 9.63% mean relative abundance in archaeal communities. Haloarchaea were relatively more abundant than methanogens in some samples. The presence of haloarchaea was also verified by fluorescence in situ hybridisation analysis. Owing to large inter-individual variations, we categorised the human gut archaeome into four archaeal enterotypes. Conclusions: The study demonstrated that the human gut archaeome is indigenous, responsive, and functional, expanding our understanding of the archaeal signature in the gut of human individuals. Video Abstract.
... s2535 (representing 5 archaeal isolates) showed > 99% 16S rRNA sequence similarity with Halococcus qingdaonensis strain CM5 isolated from a crude sea salt sample in China (Wang et al., 2007), and Halococcus sp. CBA1201 isolated from plumage of captive flamingoes in Korea (Yim et al., 2015). ...
... To the best of our knowledge Nesterenkonia, the most abundant halophile isolated in this study, is the only genus, which was not previously reported from salted skin and hide in other countries. The halophilic OTUs isolated in this study showed sequence similarities of > 98-99% with other strains previously isolated from naturally occurring saline habitats (Stan-Lotter et al., 2002;Edouard et al., 2014;Kocur and Hodgkiss, 1973;Stan-Lotter et al., 2002;Wang et al., 2009;Yilmaz, 2010;Yim et al., 2015). For example the two archaea isolates, Halococcus sp. ...
... Thus presence of visible red color on salted animal skin lead to rejection because it indicates growth of halophilic microbes that might have caused damages to the collagen fiber (Akpolat et al., 2015). Appearance of red color is a result of a red pigment produced by some halophilic archaea when grown both under natural and artificial conditions (Stan-Lotter et al., 2002;Wang et al., 2007;Yim et al., 2015). In this study, out of the 17 OTUs tested, only two archaeal isolates (representing 11.2% of the total) produced red pigments. ...
Article
Salt is widely used as preservative to protect animal skin from microbial attack. However, addition of salt creates a favorable condition for halophilic microorganisms associated with biodeterioration termed red heat damage. Knowledge about microbial diversity associated with red heat damage is expected to help develop appropriate control strategies. The objectives of this study were to isolate and characterize halophiles from salted sheepskin and evaluate their ability to degrade sheepskin. A total of 85 halophiles were isolated from salted sheepskins after enrichment in a medium containing 10%, 20% and 25% (w/v) NaCl and chopped sheepskin. In all the enrichment cultures the sheepskin was completely dissolved by the microbial consortia. Pure culture isolates belonging to the genera Halomonas, Bacillus, Salimicrobium, Nesterenkonia, and Marinococcus within Domain Bacteria and genus Halococcus from Domain Archaea were isolated. When tested independently, the isolates showed variation in their efficiency to hydrolyze sheepskin collagen. Isolate Halococcus sp. s2535 was the fastest in hydrolyzing the skin followed by Nesterenkonia sp. s2011, Marinococcus sp. s2526 and Halococcus sp. s2528. The results of this study demonstrate that halophilic microbes associated with red heat damage of salted sheepskin are highly diverse and preventive measures should target a diverse group of halophilic microbes.
... Information regarding the community-based genetic and functional traits of archaea in animal habitats is scarce. We have previously reported occurrences of diverse members of extremely halophilic archaea (haloarchaea) in avian plumage [13], as well as in food samples such as salt-fermented seafood [14] and solar salts [15,16]. In the human gut where the microbial entities thrive more abundantly than in other parts of the human body, the archaeome consisted mostly of methane-producing archaea (methanogens), of which, members belonging to the orders Methanobacteriales (i.e. ...
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Background: Archaea are one of the least-studied members of the gut-dwelling autochthonous microbiota. Few studies have reported the dominance of methanogens in the archaeal microbiome (archaeome) of the human gut, although limited information regarding the diversity and abundance of other archaeal phylotypes is available. Results: We surveyed the archaeome of faecal samples collected from 897 East Asian subjects living in South Korea. In total, 42.47% faecal samples were positive for archaeal colonisation; these were subsequently subjected to archaeal 16S rRNA gene deep sequencing and real-time quantitative polymerase chain reaction-based abundance estimation. The mean archaeal relative abundance was 10.24% ± 4.58% of the total bacterial and archaeal abundance. We observed extensive colonisation of haloarchaea (95.54%) in the archaea-positive faecal samples, with 9.63% mean relative abundance in archaeal communities. Haloarchaea were relatively more abundant than methanogens in some samples. The presence of haloarchaea was also verified by fluorescence in situ hybridisation analysis. Owing to large inter-individual variations, we categorised the human gut archaeome into four archaeal enterotypes. Conclusions: The study demonstrated that the human gut archaeome is indigenous, responsive, and functional, expanding our understanding of the archaeal signature in the gut of human individuals.
... Many Haloarchaea are facultative aerobes with the ability to grow with or without oxygen, utilizing a variety of terminal electron acceptors, and in addition they have the capacity for phototrophic growth, making them physiologically unusually versatile microorganisms Kilic et al. 2017;Mancinelli and Hochstein 1986;Martínez-Espinosa et al. 2014;Müller and DasSarma 2005;Sorokin et al. 2019;Sumper et al. 1976). Haloarchaea also are highly pigmented due to synthesis of carotenoids, resulting in bright blooms in hypersaline brine which may appear red, orange, or purple in color (DasSarma and Schwieterman 2019; de la Vega et al. 2016;Rodrigo-Baños et al. 2015;Yim et al. 2015). Coupled with our ability to isolate, construct, and characterize variants and mutants in the laboratory perturbed in their growth, pigmentation, and extremophilic properties, Haloarchaea offer the prospect of deeper insights into some fundamental questions in astrobiology. ...
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Recent progress in extremophile biology, exploration of planetary bodies in the solar system, and the detection and characterization of extrasolar planets are leading to new insights in the field of astrobiology and possible distribution of life in the universe. Among the many extremophiles on Earth, the halophilic Archaea (Haloarchaea) are especially attractive models for astrobiology, being evolutionarily ancient and physiologically versatile, potentially surviving in a variety of planetary environments and with relevance for in situ life detection. Haloarchaea are polyextremophilic with tolerance of saturating salinity, anaerobic conditions, high levels of ultraviolet and ionizing radiation, subzero temperatures, desiccation, and toxic ions. Haloarchaea survive launches into Earth’s stratosphere encountering conditions similar to those found on the surface of Mars. Studies of their unique proteins are revealing mechanisms permitting activity and function in high ionic strength, perchlorates, and subzero temperatures. Haloarchaea also produce spectacular blooms visible from space due to synthesis of red–orange isoprenoid carotenoids used for photoprotection and photorepair processes and purple retinal chromoproteins for phototrophy and phototaxis. Remote sensing using visible and infrared spectroscopy has shown that haloarchaeal pigments exhibit both a discernable peak of absorption and a reflective “green edge”. Since the pigments produce remotely detectable features, they may influence the spectrum from an inhabited exoplanet imaged by a future large space-based telescope. In this review, we focus primarily on studies of two Haloarchaea, Halobacterium sp. NRC-1 and Halorubrum lacusprofundi.
... Nevertheless, the transport of spores from one location (i.e., isolation source) to another as product of dust or winds should not be discounted. The feathers of birds like pelicans ( Kemp et al., 2018) or flamingos ( Yim et al., 2015) could also be considered as mechanical carriers (also to microbial vectors) to transport microbial cells from different habitats. In the Puna zone, where Salar de Atacama, Salar de Hombre Muerto, and Salar de Uyuni are located, three flamingo species are abundant, Phoenicopterus chilensis (Chilean), P. jamensis (James's) and P. andinus (Andean) (Hurlbert and Chang, 1983). ...
Article
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Microbial life inhabiting hypersaline environments belong to a limited group of extremophile or extremotolerant taxa. Natural or artificial hypersaline environments are not limited to high concentrations of NaCl, and under such conditions, specific adaptation mechanisms are necessary to permit microbial survival and growth. Argentina, Bolivia, and Chile include three large salars (salt flats) which globally, represent the largest lithium reserves, and are commonly referred to as the Lithium Triangle Zone. To date, a large amount of information has been generated regarding chemical, geological, meteorological and economical perspectives of these salars. However, there is a remarkable lack of information regarding the biology of these unique environments. Here, we report the presence of two bacterial strains (isolates LIBR002 and LIBR003) from one of the most hypersaline lithium-dominated man-made environments (total salinity 556 g/L; 11.7 M LiCl) reported to date. Both isolates were classified to the Bacillus genera, but displayed differences in 16S rRNA gene and fatty acid profiles. Our results also revealed that the isolates are lithium-tolerant and that they are phylogenetically differentiated from those Bacillus associated with high NaCl concentration environments, and form a new clade from the Lithium Triangle Zone. To determine osmoadaptation strategies in these microorganisms, both isolates were characterized using morphological, metabolic and physiological attributes. We suggest that our characterization of bacterial isolates from a highly lithium-enriched environment has revealed that even at such extreme salinities with high concentrations of chaotropic solutes, scope for microbial life exists. These conditions have previously been considered to limit the development of life, and our work extends the window of life beyond high concentrations of MgCl 2 , as previously reported, to LiCl. Our results can be used to further the understanding of salt tolerance, most especially for LiCl-dominated brines, and likely have value as models for the understanding of putative extra-terrestrial (e.g., Martian) life.
... Since halophilic archaea can survive over geologic time in halite [2,[7][8][9][10][11][12][13][14][15][16][17][18][19][20][21], and these crystals would likely form on feathers of birds feeding in GSL waters, we decided to investigate the ability of halophilic archaea in halite to be carried mechanically by migrating birds. Birds as vectors for haloarchaeal dispersal have been suggested by some studies on geographic distribution [10,64,65] and shown by two: a Halococcus species was found in salt crystals collected from the nostril salt gland of a migratory bird [66] and a broad diversity of halophilic archaea were discovered on flamingo feathers [67]. In this report, we present evidence for the formation of halite crystals on feathers and their preservation of halophilic archaea. ...
... However, a pattern of connecting overlapping migration routes for distribution, with the premise that halophilic archaea can hitchhike on one bird and be picked up at the next location by another, is plausible. The recent study on halophilic archaea transport by flamingoes underscores this principle [67]. Avian migration routes are typically within the flowing airspace of the troposphere where they travel 10-15 m/s, and the moving winds may even surpass this speed, impacting flightpaths [153,154]. ...
Article
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Halophilic archaea inhabit hypersaline ecosystems globally, and genetically similar strains have been found in locales that are geographically isolated from one another. We sought to test the hypothesis that small salt crystals harboring halophilic archaea could be carried on bird feathers and that bird migration is a driving force of these distributions. In this study, we discovered that the American White Pelicans (AWPE) at Great Salt Lake soak in the hypersaline brine and accumulate salt crystals (halite) on their feathers. We cultured halophilic archaea from AWPE feathers and halite crystals. The microorganisms isolated from the lakeshore crystals were restricted to two genera: Halorubrum and Haloarcula, however, archaea from the feathers were strictly Haloarcula. We compared partial DNA sequence of the 16S rRNA gene from our cultivars with that of similar strains in the GenBank database. To understand the biogeography of genetically similar halophilic archaea, we studied the geographical locations of the sampling sites of the closest-matched species. An analysis of the environmental factors of each site pointed to salinity as the most important factor for selection. The geography of the sites was consistent with the location of the sub-tropical jet stream where birds typically migrate, supporting the avian dispersal hypothesis.
... Euryarchaeota microorganisms are mainly aerobic heterotrophs that can also obtain energy from light due to bacteriorhodopsin. They are characteristically halophiles, and some of them are also resistant to hyperhaline conditions and provide the red pigmentation in the plumage of flamingos (Yim et al. 2015). ...
Article
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Flamingos Phoenicopteridae sp. are gregarious birds that travel long distances between breeding and feeding sites. Here we describe the diet and feeding selectivity of two flamingo species, the Andean Flamingo Phoenicoparrus andinus and Chilean Flamingo Phoenicopterus chilensis, which coexist in a lowland area of Argentina. Environmental characteristics and available food resources were assessed at twelve lakes where feeding flocks of both species of flamingos occurred. Food items found in faeces (16S rRNA for bacteria and archaea) and microscopic analyses (for Cyanobacteria, microalgae and microinvertebrates) were analysed, and the birds' feeding selectivity and niche overlap were estimated. Results showed that the lakes were of eutrophic to hypereutrophic status, and with hypohaline to mesohaline salinity levels. Predominant microorganisms belonged to the Planctomycetes, Verrucomicrobia, Chloroflexi, Euryarchaeota, Cyanobacteria, Bacillariophyta and Copepoda phyla. Euryarchaeota and Firmicutes were the main phyla found in the faeces, with Chloroflexi and Planctomycetes also present in smaller quantities. Proteobacteria were well represented in Andean Flamingo faeces, but Verrucomicrobia were scarce in both species. Cyanobacteria, Bacillariophyta,