Sens­ing Blue Light: From Bac­te­ria to Birds

by Me­chas 

That many birds mi­grate over long dis­tances is a well-known fact. But read­ing the book "World on the Wing: The Global Odyssey of Mi­gra­tory Birds" by Scott Wei­den­saul proved to be a true eye-opener. I also learned a fact that re­ally stuck with me. When fly­ing for re­mark­ably long dis­tances, of­ten many thou­sands of kilo­me­ters over open oceans, birds sense the Earth's mag­netic field to help ori­ent them­selves. They ac­com­plish this through the ef­fect of light on pro­teins called cryp­tochromes. Not hav­ing heard of these pro­teins be­fore I was in­trigued. How can they en­able mag­netic per­cep­tion?

Fig. 1. Light re­ac­tions rel­e­vant for CPD (cy­clobutyl pyri­midine dimer) pho­tolyase. Green and red boxes in­di­cate in­tact and dam­aged DNA, re­spec­tively. T=T is a CPD formed from two thymines. Yel­low and blue el­lipses in­di­cate pho­tolyase with flavin in fully re­duced (FADH–) and semi-re­duced state (FADH•), re­spec­tively. Source. Fron­tispiece: A flock of Bar-tailed God­wit land­ing (Limosa lap­pon­ica), Oriel­ton La­goon, Tas­ma­nia, Aus­tralia. Source

In many plants and an­i­mals, some types of cryp­tochromes func­tion as blue-light-sen­si­tive pho­tore­cep­tors. As such, they are im­por­tant for cir­ca­dian rhythm reg­u­la­tion in Ara­bidop­sis thaliana and the fruit fly Drosophila melanogaster. But cryp­tochromes are mem­bers of a large and very widely dis­trib­uted pro­tein fam­ily whose mem­bers have dif­fer­ent func­tions. Most strik­ingly, cryp­tochromes share ex­ten­sive se­quence sim­i­lar­ity with pho­tolyases, pro­teins that con­tain the co­fac­tor flavin ade­nine din­u­cleotide (FAD) and re­pair DNA dam­age in­duced by "far UV" light (wave­lengths <300 nM). The pre­dom­i­nant form of UV dam­age on DNA is the for­ma­tion of "cy­clobutyl pyrim­i­dine dimers" (CPDs) at ad­ja­cent pyrim­idines (Fig­ure 1). Upon ex­ci­ta­tion by "near UV"/blue light (wave­lengths 300–450 nM) the pho­tolyase-FAD en­zyme trans­fers the elec­trons that are needed to split the pyrim­i­dine dimers and re­pair UV-dam­aged DNA. This is known as pho­tore­ac­ti­va­tion, an evo­lu­tion­ar­ily an­cient mech­a­nism that prob­a­bly arose in early Earth be­fore the for­ma­tion of the ozone layer. It's an ef­fi­cient way to re­verse the dam­age of UV-light with the aid of blue light. Pho­tore­ac­ti­va­tion is a con­served mech­a­nism in many or­gan­isms, from bac­te­ria to plants, fungi, and an­i­mals. But hu­mans and other pla­cen­tal mam­mals have lost it and re­placed it with the less ef­fi­cient nu­cleotide ex­ci­sion re­pair.

Fig 2. Do­mains of the cryptochrome/photolyase (CRY/ PHR) su­per­fam­ily. The ref­er­ence se­quences cor­re­spond to: An­i­mal CRY, Homo sapi­ens CRY1 (NP_004066); plant CRY, Ara­bidop­sis thaliana CRY1 (NP_567341); CRY-DASH, Xeno­pus lae­vis (NP_001084438); (6–4) PHR, Danio re­rio (NP_571863); CPD PHR, D. re­rio CPD class II PHR (NP_957358). The DNA pho­tolyase re­lated do­main and a FAD bind­ing do­main are shared by both CRY and PHR, whereas the C‑terminal vari­able do­main is only present in CRY but not in PHR. Source

Pho­tolyases and cryp­tochromes are evo­lu­tion­ar­ily re­lated but can be sub­di­vided into sev­eral sub­fam­i­lies based on the ex­tent of their se­quence sim­i­lar­ity. They also dif­fer in the dis­tri­b­u­tion of do­mains within the pro­tein, do­mains that turn out to be very im­por­tant for their func­tion (Fig­ure 2). They all pos­sess a pho­tolyase-re­lated re­gion and a do­main in­volved in bind­ing FAD, but pho­tolyases lack a vari­able C‑terminal do­main found in cryp­tochromes. In ad­di­tion, there is a group of pro­teins whose se­quences place them phy­lo­ge­net­i­cally "in be­tween" pho­tolyases and cryp­tochromes. These pro­teins are called Cry-DASH and have di­verse func­tions in or­gan­isms rang­ing from ar­chaea to ver­te­brates. Like pho­tolyases, CRY-DASHs are in­volved in re­pair of DNA, but they tar­get sin­gle-stranded rather than dou­ble-stranded DNA. Like cryp­tochromes, CRY-DASHs can func­tion as pho­tore­cep­tors in or­gan­isms such as fungi and in the cyanobac­terium Syne­chocys­tis. This in be­tween group thus seems to pro­vide the miss­ing link be­tween the evo­lu­tion of re­pair and reg­u­la­tory func­tions.

Fig. 3. Pro­posed Mech­a­nism for Quan­tum Magneto­reception in Birds. Cryp­tochrome in cells in the retina of the eye ab­sorb blue light and form rad­i­cal pairs of elec­trons which can spin ei­ther in op­po­si­tion or in par­al­lel, pro­vid­ing an ex­tremely sen­si­tive quan­tum de­tec­tor for the Earth's weak mag­netic field. The di­rec­tion of the field in­flu­ences the pro­por­tion of the cy­tochrome mol­e­cules that en­ter dif­fer­ent states. The di­rec­tion is sig­naled via a cas­cade of neu­ro­trans­mit­ter mol­e­cules, and then to the brain via nerve im­pulses in the op­tic nerve. By Chiswick Chap — Own work, CC BY-SA 4.0. Source

How pho­tolyases and cryp­tochromes evolved to carry out their dif­fer­ent light-de­pen­dent func­tions is un­clear. As men­tioned be­fore, their ca­pac­ity to sense blue light is a fea­ture that likely evolved very early in Earth's his­tory. Thus, plant and an­i­mal cryp­tochromes prob­a­bly evolved from some an­ces­tral pho­tolyases. One of the most fas­ci­nat­ing adap­ta­tions is, un­doubt­edly, the in­volve­ment of cryp­tochromes in bird nav­i­ga­tion. Nu­mer­ous species, some of them tiny song­birds, travel non-stop for thou­sands of miles us­ing ce­les­tial cues and the Earth's mag­netic fields to skill­fully nav­i­gate the skies. How these an­i­mals com­plete these jour­neys is still not fully un­der­stood, but the cur­rent pro­posal in­volves cryp­tochromes in the birds' eyes (Fig­ure 3). When ac­ti­vated by blue light an elec­tron-trans­fer re­ac­tion oc­curs be­tween the FAD co-fac­tor and sev­eral tryp­to­phan residues lo­cated nearby within the cryp­tochrome. This re­ac­tion gen­er­ates rad­i­cal pairs with quan­tum ef­fects (yes, this in­volves quan­tum me­chan­ics!) that can sense the Earth's weak mag­netic fields. In a way, it ap­pears that bird's eyes can "see" mag­netic fields, giv­ing a com­pletely new mean­ing to the phrase "from a bird's eye view." This may sound bizarre and im­mensely com­plex, but it is cur­rently the pre­ferred ex­pla­na­tion. And this ex­quis­ite bi­o­log­i­cal func­tion is tied to and de­rived from those an­ces­tral mi­crobes that used blue light to re­pair DNA dam­age. But in birds this as­ton­ish­ing adap­ta­tion pro­vides them with the en­vi­able ca­pac­ity to find their way around the globe, free of com­passes or GPS, us­ing cues that we hu­mans sim­ply can't per­ceive.

 

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