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Sequences belonging to the genera Haloquadratum Hqr. Carotenoids from isolated haloarchaea, red flamingo feathers, and assorted artificial feed were analyzed by micro-Raman spectroscopy. Consistent Raman spectra were obtained across replicates for each type of sample, with only minor shifts within each group. The haloarchaeal strains and feathers showed similar profiles, whereas the spectrum for feed samples differed Fig.

Although the typical major peaks in the Raman spectra are consistent with the presence of bacterioruberin, they do not prove its presence in feather samples, since other carotenoids could exhibit similar resonances due to the low spectral resolution of Raman spectroscopy To confirm the presence of specific haloarchaeal carotenoids such as bacterioruberin or its precursors monoanhydrobacterioruberin MABR , bisanhydrobacterioruberin BABR , and isopentenyldehydrorhodopin IDR 29 in the feather samples, carotenoid pigments extracted from feathers, haloarchaea, and feed, together with the appropriate standards, cyanobacterial carotenoid echinenone , and microalgal carotenoid astaxanthin were analyzed by Ultra Performance Liquid Chromatography UPLC.

The second peak obtained from the haloarchaeal strains, with a retention time of 7. This study was based on the observation that flamingo plumage displays elegant colors similar to haloarchaeal carotenoid-based pigments. The viable red-colored haloarchaea belonging to the genera Halococcus and Halogeometricum were cultured and isolated directly from the feathers of flamingoes in captivity, using a culture-dependent approach. This is the first report of viable extremophilic archaea present in avian plumage, and provides a novel perspective on fundamental aspects of feather microbiology.

Haloarchaea are currently classified into 48 genera with species in the List of Prokaryotic Names with Standing in Nomenclature database Species of the Hcc. Culture-independent approach was also applied to investigate detailed haloarchaeal community structures in the flamingo feathers from which the haloarchaeal strains were isolated. A culture-independent approach that circumvents PCR amplicon sequencing biases using a next-generation sequencing platform was also applied to metagenomes obtained from flamingo feathers where the haloarchaeal strains were isolated to investigate detailed haloarchaeal community structure.

Metagenomic analysis of flamingo feathers showed 13 haloarchaeal genera and unclassified sequences of the class Halobacteria at the genus level. It is interesting that no isolated Halococcus -related phylotypes were found in the metagenome sequences; it is possible that this discrepancy between culture-dependent and culture-independent data is caused by inefficient breakage of the thick polysaccharide layer in the cell walls of the Halococcus spp. The halotolerant Bacillus strain 2—9—3, isolated from a million-year-old salt crystal, has been reported in as the oldest viable organism Since then, several criteria for ensuring the authenticity of isolates or DNA from novel and unusual places have been outlined in the course of the debate on the isolation of ancient DNA 33 , The presence of haloarchaea in the plumage of birds reported in this study could constitute a comparable microbiological issue since the existence of haloarchaea in bird feathers has not been previously demonstrated.


The authenticity of the haloarchaeal isolates is supported by the following points regarding intra-laboratory contamination. First, the haloarchaea were isolated with extreme care and based on extensive hands-on experience with haloarchaeal cultivation. Moreover, the haloarchaea were successfully isolated only from the feather samples, but not from either pond water or soil samples in the flamingo cage.

Second, none of the archaeal strains present in our laboratory are identical to the haloarchaea isolated from the feathers, as determined based on 16S rRNA gene sequences. In addition, other evidence of the presence of haloarchaea in the feathers was obtained from metagenomic sequencing of DNA extracts showing diverse haloarchaeal phylotypes. Flamingoes at the zoo were fed mainly an assortment of artificial food from which no haloarchaeal strains were isolated.

In addition, the birds were not exposed to hypersaline environments since they were imported; it was therefore possible that the flamingoes had transported the haloarchaeal cells from their native hypersaline habitats. It was also suggested that Cyanobacteria migrate between different habitats via Lesser flamingoes Flamingoes are social birds that live in colonies that can include thousands of individuals, have a behavior to rub the feathers with their heads, and drink water and wash their feathers in saline waters where haloarchaea thrive.

Thus, haloarchaeal cells may adhere to feathers and be transferred between individuals by physical contact. There is some overlap in the global distribution of flamingoes and haloarchaea isolation sites Fig.

Flamingo Photography: How to Capture Great Photos of Flamingos

The flamingoes mostly inhabit seashores or salt and soda lakes and haloarchaea were isolated from hypersaline environments such as salt lakes and solar salterns whose salt concentrations fit the growth conditions of haloarchaea. For example, Hrr. In addition, Halomicrobium katesii 42 and Hrr. Flamingo habitats are indicated by a pink color and haloarchaeal sites are shown by blue triangles. The sources of haloarchaeal isolation sites can be found in Supplementary Information. For verification of correlation between pigments of flamingo plumage and the isolated haloarchaea, carotenoid-based pigments from the red flamingo feathers and haloarchaea were analyzed using Raman spectroscopy and UPLC.

Plumage pigments have been characterized in swallows, bluebirds, penguins, chickens 44 , 45 , parrots 46 , 47 , and mallards 48 , and mostly consist of melanins and carotenoids 3 , While the former are synthesized independently of ingested nutrients, carotenoids—which emerged in archaea as lipophilic biochemicals reinforcing cell membranes and serving as antioxidants and confer a red, orange, or yellow color to avian feathers—are only acquired by ingestion of carotenoid feeding 1 , 3 , 5.

The pink or reddish colors of flamingo plumage originated from the carotenoids by carotenoid-abundant feed often in hypersaline lakes where is one of the haloarchaeal habitats. Carotenoid-based plumage coloration occurs through a mechanism involving carotenoid transport to blood and uptake by follicle cells in feathers 1 , 50 , 51 , Analysis of the major carotenoid pigments of haloarchaea 21 , 22 , 23 , 24 , 25 , 29 revealed that the isoprenoid-derived carotenoids, bacterioruberin and its precursors, are present in the haloarchaea membrane, giving rise to the characteristic bright pinkish-red color.

In this study, haloarchaeal community structures in red flamingo feathers were analyzed by culture-dependent and culture-independent approaches. The unusual existence of the extremophilic archaea in the avian plumage can provide fundamental insight to the feather microbiologist, as well as birder and ornithologist.

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The bacterioruberin precursor responsible for the red coloration of haloarchaea was consistent with one of the carotenoid pigments found in flamingo feathers. The carotenoid-based plumage coloration of the molting flamingoes that have been mostly fed the restricted diet without the carotenoid pigments at the zoo is not explained satisfactorily with the known coloration mechanisms. The coincidence of the carotenoid-based pigments in the haloarchaeal cells and the avian feathers suggests that haloarchaea may be considered as an environmental factor affecting the plumage coloration.

The biological significances of the findings as well as the possible mechanisms for carotenoid-based plumage coloration by microorganisms need to be investigated in future studies. Chilean Phoenicopterus chilensis , Lesser P. Most of the flamingoes were imported from Cuba in and still remain in the same cage, and there were no records of the countries of origin for the remaining individuals.

Flamingo feathers were randomly collected from the birds and these along with the feed were transported directly to the laboratory. The animal breeding protocols were approved by the institutional committee of the Seoul Zoo of Grand Park and the sampling methods were carried out in accordance with the approved guidelines.

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The pH of the media was adjusted to pH 7. Flamingo feathers 0. Colonies were transferred to fresh plates at least three times in order to obtain a pure culture. The isolated strains were cultured on various media and their growth capacity was determined. Nucleotide similarity values were calculated using EzTaxon-e server Microbial community analysis was carried out using the metagenomics RAST server For carotenoid analysis, cells from isolated haloarchaeal strains, red flamingo feathers, and commercial feed were lyophilized, and carotenoid content was analyzed in triplicate for each sample by micro-Raman spectroscopy Nanofinder 30; Tokyo Instruments, Tokyo, Japan according to a previously described method 21 with the following modifications: a nm laser was used for excitation at a laser power of 2.

Carotenoids were extracted under dim light from three randomly selected haloarchaeal strains and commercial feed according to a previously described method 63 with some modifications. Samples 0. Carotenoid extraction from red feathers was performed under dim light as follows: the feathers were ground using liquid nitrogen and the ground sample 0.

The flow rate was set at 0.

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The metagenome sequences of the flamingo feathers have been deposited in the MG-RAST server under accession numbers How to cite this article : Yim, K. Occurrence of viable, red-pigmented haloarchaea in the plumage of captive flamingoes. E , and by a project fund C to J. The authors would like to thank Dr. Michael L. Dyall-Smith for providing constructive advices. Author Contributions S. They offer photographers a goldmine of opportunities. Whether you have a chance to meet them in the wild, or have the limited access afforded by zoos, use patience, look the birds in the eye, and have fun.

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Bio Latest Posts. Jennifer Berube. Jennifer Berube is a freelance writer and photographer with a background in journalism. She contributes regularly to PictureCorrect. Latest posts by Jennifer Berube see all. Most popular posts in July. Most recent. Connect with:.

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