Homochirality is a generic and unique property of all biochemical life and it is considered a universal and agnostic biosignature. Upon interaction with unpolarized light, homochirality induces fractional circular polarization in the light that is scattered from it, which can be sensed remotely. As such, it can be a prime candidate biosignature in the context of future life detection missions and observatories. The linear polarizance of vegetation is also sometimes envisaged as a biosignature, although it does not share the same molecular origin as circular polarization. It is known that linear polarization of surfaces is strongly dependent on the phase angle. The relationship between the phase angle and circular polarization stemming from macromolecular assemblies such as in vegetation, however, remained unclear. In this study, using the average of 27 different species, we demonstrate that the circular polarization–phase angle dependency of vegetation induces relatively small changes in spectral shape and mostly affects the signal magnitude. With these results, we underline the use of circular spectropolarimetry as a promising agnostic biosignature complementary to the use of linear spectropolarimetry and scalar reflectance.
Get full access to this article
View all access options for this article.
References
1.
AvnirD.Critical review of chirality indicators of extraterrestrial life. New Astron Rev, 2021; 92:101596; doi: 10.1016/j.newar.2020.101596.
2.
BarzdaV, MustardyL, GarabG.Size dependency of circular dichroism in macroaggregates of photosynthetic pigment-protein complexes. Biochemistry, 1994; 33(35):10837–10841; doi: 10.1021/bi00201a034.
3.
BerdyuginaSV, KuhnJR, HarringtonDM, et al. Remote sensing of life: Polarimetric signatures of photosynthetic pigments as sensitive biomarkers. Int J Astrobiol, 2016; 15(1):45–56; doi: 10.1017/S1473550415000129.
4.
BonnerWA.Chirality and life. Orig Life Evol Biosph, 1995; 25(1–3):175–190; doi: 10.1007/BF01581581.
5.
BustamanteC, TinocoI, MaestreMF. Circular differential scattering can be an important part of the circular dichroism of macromolecules. Proc Natl Acad Sci U S A, 1983; 80(12):3568–3572; doi: 10.1073/pnas.80.12.3568.
6.
BustamanteC, MaestreMF, KellerD.Expressions for the interpretation of circular intensity differential scattering of chiral aggregates. Biopolymers, 1985; 24(8):1595–1612; doi: 10.1002/bip.360240813.
7.
FasmanGD.Circular Dichroism and the Conformational Analysis of Biomolecules. Springer Science & Business Media: Amsterdam; 2013.
8.
FinziL, BustamanteC, GarabG, et al. Direct observation of large chiral domains in chloroplast thylakoid membranes by differential polarization microscopy. Proc Natl Acad Sci U S A, 1989; 86(22):8748–8752; doi: 10.1073/pnas.86.22.8748.
9.
GarabG.Linear and circular dichroism. In: Biophysical Techniques in Photosynthesis. (Amesz J, Hoff AJ. eds.) Kluwer Academic Publishers: Dordrecht, 1996; pp. 11–40.
10.
GarabG, Faludi-DanielA, SutherlandJC, et al. Macroorganization of chlorophyll a/b light-harvesting complex in thylakoids and aggregates: Information from circular differential scattering. Biochemistry, 1988a;27(7):2425–2430; doi: 10.1021/bi00407a027.
11.
GarabG, WellsS, FinziL, et al. Helically organized macroaggregates of pigment-protein complexes in chloroplasts: Evidence from circular intensity differential scattering. Biochemistry, 1988b;27(16):5839–5843; doi: 10.1021/bi00416a003.
12.
GarabG, FinziL, BustamanteC.Differential polarization imaging of chloroplasts: Microscopic and macroscopic linear and circular dichroism. In: Light in Biology and Medicine, Volume 2 (Douglas RH. ed.) Plenum Press: New York, 1991; pp. 77–88.
13.
GarabG, van AmerongenH.Linear dichroism and circular dichroism in photosynthesis research. Photosynth Res, 2009; 101(2–3):135–146, doi: 10.1007/s11120-009-9424-4.
14.
GrantL.Diffuse and specular characteristics of leaf reflectance. Remote Sens Environ, 1987; 22(2):309–322; doi: 10.1016/0034-4257(87)90064-2.
15.
GrantL, DaughtryCST, VanderbiltVC. Polarized and specular reflectance variation with leaf surface features. Physiol Plant, 1993; 88(1):1–9; doi: 10.1111/j.1399-3054.1993.tb01753.x.
16.
GrishinDV, ZhdanovDD, PokrovskayaMV, et al. D-amino acids in nature, agriculture and biomedicine. All Life, 2020; 13(1):11–22; doi: 10.1080/21553769.2019.1622596.
17.
GrootA, RossiL, TreesVJH, et al. Colors of an Earth-like exoplanet-temporal flux and polarization signals of the Earth. Astron Astrophys, 2020; 640:A121; doi: 10.1051/0004-6361/202037569.
18.
JacquemoudS, UstinS.Measurement of leaf optical properties. In: Leaf Optical Properties. (Jacquemoud S, Ustin S. eds.) Cambridge University Press: Cambridge, United Kingdom, 2019; pp. 74–123.
19.
JafarpourF, BiancalaniT, GoldenfeldN.Noise-induced mechanism for biological homochirality of early life self-replicators. Phys Rev Lett, 2015; 115(15):158101; doi: 10.1103/PhysRevLett.115.158101.
20.
KellerD, BustamanteC.Theory of the interaction of light with large inhomogeneous molecular aggregates. II. Psi-type circular dichroism. J Chem Phys, 1986; 84(6):2972–2980; doi: 10.1063/1.450278.
21.
KempJC, HensonGD, SteinerCT, et al. The optical polarization of the Sun measured at a sensitivity of parts in ten million. Nature, 1987; 326(6110):270–273; doi: 10.1038/326270a0.
22.
KlindžićD, StamD, SnikF, et al. LOUPE: Observing the Earth from the Moon to prepare for detecting life on Earth-like exoplanets. Philos Trans A Math Phys Eng Sci, 2021; 379(2188); doi: 10.1098/rsta.2019.0577.
23.
LambrevPH, AkhtarP.Macroorganisation and flexibility of thylakoid membranes. Biochem J, 2019; 476(20):2981–3018; doi: 10.1042/BCJ20190080.
24.
MacDermottAJ.8.2 Perspective and concepts: Biomolecular significance of homochirality: The origin of the homochiral signature of life. In: Comprehensive Chirality, edited by EM Carreira and H Yamamoto. Elsevier: Amsterdam, 2012; pp. 11–38.
25.
NovotnyM, KleywegtGJ. A survey of left-handed helices in protein structures. J Mol Biol, 2005; 347(2):231–241; doi: 10.1016/j.jmb.2005.01.037.
26.
PattyCHL, VisserLJJ, ArieseF, et al. Circular spectropolarimetric sensing of chiral photosystems in decaying leaves. J Quant Spectrosc Radiat Transf, 2017; 189:303–311; doi: 10.1016/j.jqsrt.2016.12.023.
27.
PattyCHL, ArieseF, BumaWJ, et al. Circular spectropolarimetric sensing of higher plant and algal chloroplast structural variations. Photosynth Res, 2018a;140(2):129–139; doi: 10.1007/s11120-018-0572-2.
28.
PattyCHL, LuoDA, SnikF, et al. Imaging linear and circular polarization features in leaves with complete Mueller matrix polarimetry. Biochim Biophys Acta General Subjects, 2018b;1862(6):1350–1363; doi: 10.1016/j.bbagen.2018.03.005.
29.
PattyCHL, ten KateIL, SparksWB, et al. Remote sensing of homochirality: A proxy for the detection of extraterrestrial life. In: Chiral Analysis, Second Edition: Advances in Spectroscopy, Chromatography and Emerging Methods. (Polavarapu P. ed.) Elsevier Science: Amsterdam, 2018c; pp. 29–69.
30.
PattyCHL, ten KateIL, BumaWJ, et al. Circular spectropolarimetric sensing of vegetation in the field: Possibilities for the remote detection of extraterrestrial life. Astrobiology, 2019; 19(10):1221–1229; doi: 10.1089/ast.2019.2050.
31.
PattyCHL, Ku¨hnJG, LambrevPH, et al. Biosignatures of the Earth I. Airborne spectropolarimetric detection of photosynthetic life. Astron Astrophys, 2021; 651:A68; doi: 10.1051/0004-6361/202140845.
32.
PeltoniemiJI, GritsevichM, PuttonenE.Reflectance and Polarization Characteristics of Various Vegetation Types. Springer Nature: Berlin; 2015.
33.
PopaR.Between Necessity and Probability: Searching for the Definition and Origin of Life. Springer Science & Business Media: Berlin; 2004.
SparksWB, HoughJ, GermerTA, et al. Detection of circular polarization in light scattered from photosynthetic microbes. Proc Natl Acad Sci U S A, 2009; 106(19):7816–7821; doi: 10.1073/pnas.0810215106.
36.
SparksWB, ParenteauMN, BlankenshipRE, et al. Spectropolarimetry of primitive phototrophs as global surface biosignatures. Astrobiology, 2021; 21(2):219–234; doi: 10.1089/ast.2020.2272.
37.
UmovNA.Chromatische depolarisation durch lichtzerstreuung. Phys Z, 1905; 6:674–676.
38.
VanderbiltVC, GrantL, DaughtryCST. Polarization of light scattered by vegetation. Proc IEEE, 1985; 73(6):1012–1024; doi: 10.1109/PROC.1985.13232.
39.
VanderbiltVC, GrantL, UstinSL. Polarization of light by vegetation. In: Photon-Vegetation Interactions. (Myneni RB. ed.) Springer: Berlin, 1991; pp. 191–228.
40.
VanderbiltVC, DaughtryCST, KupinskiMK, et al. Estimating the relative water content of leaves in a cotton canopy. Proc SPIE, 2017; 10407:104070Z; doi: 10.1117/12.2274502.
WaldG.The origin of optical activity. Ann NY Acad Sci, 1957; 69(2):352–368; doi: 10.1111/j.1749-6632.1957.tb49671.x.
43.
YaoC, LuS, SunZ.Estimation of leaf chlorophyll content with polarization measurements: Degree of linear polarization. J Quant Spectrosc Radiat Transf, 2020; 242:106787; doi: 10.1016/j.jqsrt.2019.106787.
Supplementary Material
Please find the following supplemental material available below.
For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.
For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.
