Dynamic pigmentary and structural coloration within cephalopod chromatophore organs

Thomas L. Williams; Stephen L. Senft; Jingjie Yeo; Francisco J. Martín-Martínez; Alan M. Kuzirian; Camille A. Martin; Christopher W. DiBona; Chun Teh Chen; Sean R. Dinneen; Hieu T. Nguyen; Conor M. Gomes; Joshua J.C. Rosenthal; Matthew D. MacManes; Feixia Chu; Markus J. Buehler; Roger T. Hanlon; Leila F. Deravi

doi:10.1038/s41467-019-08891-x

Dynamic pigmentary and structural coloration within cephalopod chromatophore organs

Thomas L. Williams, Stephen L. Senft, Jingjie Yeo, Francisco J. Martín-Martínez, Alan M. Kuzirian, Camille A. Martin, Christopher W. DiBona, Chun Teh Chen, Sean R. Dinneen, Hieu T. Nguyen, Conor M. Gomes, Joshua J.C. Rosenthal, Matthew D. MacManes, Feixia Chu, Markus J. Buehler, Roger T. Hanlon, Leila F. Deravi^*

^*Corresponding author for this work

Chemistry

Research output: Contribution to journal › Article › peer-review

118 Citations (Scopus)

Abstract

Chromatophore organs in cephalopod skin are known to produce ultra-fast changes in appearance for camouflage and communication. Light-scattering pigment granules within chromatocytes have been presumed to be the sole source of coloration in these complex organs. We report the discovery of structural coloration emanating in precise register with expanded pigmented chromatocytes. Concurrently, using an annotated squid chromatophore proteome together with microscopy, we identify a likely biochemical component of this reflective coloration as reflectin proteins distributed in sheath cells that envelop each chromatocyte. Additionally, within the chromatocytes, where the pigment resides in nanostructured granules, we find the lens protein Ω- crystallin interfacing tightly with pigment molecules. These findings offer fresh perspectives on the intricate biophotonic interplay between pigmentary and structural coloration elements tightly co-located within the same dynamic flexible organ - a feature that may help inspire the development of new classes of engineered materials that change color and pattern.

Original language	English
Article number	1004
Journal	Nature Communications
Volume	10
Issue number	1
DOIs	https://doi.org/10.1038/s41467-019-08891-x
Publication status	Published - 1 Dec 2019

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Williams, T. L., Senft, S. L., Yeo, J., Martín-Martínez, F. J., Kuzirian, A. M., Martin, C. A., DiBona, C. W., Chen, C. T., Dinneen, S. R., Nguyen, H. T., Gomes, C. M., Rosenthal, J. J. C., MacManes, M. D., Chu, F., Buehler, M. J., Hanlon, R. T., & Deravi, L. F. (2019). Dynamic pigmentary and structural coloration within cephalopod chromatophore organs. Nature Communications, 10(1), Article 1004. https://doi.org/10.1038/s41467-019-08891-x

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title = "Dynamic pigmentary and structural coloration within cephalopod chromatophore organs",

abstract = "Chromatophore organs in cephalopod skin are known to produce ultra-fast changes in appearance for camouflage and communication. Light-scattering pigment granules within chromatocytes have been presumed to be the sole source of coloration in these complex organs. We report the discovery of structural coloration emanating in precise register with expanded pigmented chromatocytes. Concurrently, using an annotated squid chromatophore proteome together with microscopy, we identify a likely biochemical component of this reflective coloration as reflectin proteins distributed in sheath cells that envelop each chromatocyte. Additionally, within the chromatocytes, where the pigment resides in nanostructured granules, we find the lens protein Ω- crystallin interfacing tightly with pigment molecules. These findings offer fresh perspectives on the intricate biophotonic interplay between pigmentary and structural coloration elements tightly co-located within the same dynamic flexible organ - a feature that may help inspire the development of new classes of engineered materials that change color and pattern.",

author = "Williams, {Thomas L.} and Senft, {Stephen L.} and Jingjie Yeo and Mart{\'i}n-Mart{\'i}nez, {Francisco J.} and Kuzirian, {Alan M.} and Martin, {Camille A.} and DiBona, {Christopher W.} and Chen, {Chun Teh} and Dinneen, {Sean R.} and Nguyen, {Hieu T.} and Gomes, {Conor M.} and Rosenthal, {Joshua J.C.} and MacManes, {Matthew D.} and Feixia Chu and Buehler, {Markus J.} and Hanlon, {Roger T.} and Deravi, {Leila F.}",

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Williams, TL, Senft, SL, Yeo, J, Martín-Martínez, FJ, Kuzirian, AM, Martin, CA, DiBona, CW, Chen, CT, Dinneen, SR, Nguyen, HT, Gomes, CM, Rosenthal, JJC, MacManes, MD, Chu, F, Buehler, MJ, Hanlon, RT & Deravi, LF 2019, 'Dynamic pigmentary and structural coloration within cephalopod chromatophore organs', Nature Communications, vol. 10, no. 1, 1004. https://doi.org/10.1038/s41467-019-08891-x

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AU - Williams, Thomas L.

AU - Senft, Stephen L.

AU - Yeo, Jingjie

AU - Martín-Martínez, Francisco J.

AU - Kuzirian, Alan M.

AU - Martin, Camille A.

AU - DiBona, Christopher W.

AU - Chen, Chun Teh

AU - Dinneen, Sean R.

AU - Nguyen, Hieu T.

AU - Gomes, Conor M.

AU - Rosenthal, Joshua J.C.

AU - MacManes, Matthew D.

AU - Chu, Feixia

AU - Buehler, Markus J.

AU - Hanlon, Roger T.

AU - Deravi, Leila F.

PY - 2019/12/1

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N2 - Chromatophore organs in cephalopod skin are known to produce ultra-fast changes in appearance for camouflage and communication. Light-scattering pigment granules within chromatocytes have been presumed to be the sole source of coloration in these complex organs. We report the discovery of structural coloration emanating in precise register with expanded pigmented chromatocytes. Concurrently, using an annotated squid chromatophore proteome together with microscopy, we identify a likely biochemical component of this reflective coloration as reflectin proteins distributed in sheath cells that envelop each chromatocyte. Additionally, within the chromatocytes, where the pigment resides in nanostructured granules, we find the lens protein Ω- crystallin interfacing tightly with pigment molecules. These findings offer fresh perspectives on the intricate biophotonic interplay between pigmentary and structural coloration elements tightly co-located within the same dynamic flexible organ - a feature that may help inspire the development of new classes of engineered materials that change color and pattern.

AB - Chromatophore organs in cephalopod skin are known to produce ultra-fast changes in appearance for camouflage and communication. Light-scattering pigment granules within chromatocytes have been presumed to be the sole source of coloration in these complex organs. We report the discovery of structural coloration emanating in precise register with expanded pigmented chromatocytes. Concurrently, using an annotated squid chromatophore proteome together with microscopy, we identify a likely biochemical component of this reflective coloration as reflectin proteins distributed in sheath cells that envelop each chromatocyte. Additionally, within the chromatocytes, where the pigment resides in nanostructured granules, we find the lens protein Ω- crystallin interfacing tightly with pigment molecules. These findings offer fresh perspectives on the intricate biophotonic interplay between pigmentary and structural coloration elements tightly co-located within the same dynamic flexible organ - a feature that may help inspire the development of new classes of engineered materials that change color and pattern.

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Dynamic pigmentary and structural coloration within cephalopod chromatophore organs

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