Several aspects of the proposal, which aims to expand open access, require serious discussion and, in some cases, a rethink.
Image credit: Dave Cutler (artist).
New Research In
Physical Sciences
Featured Portals
Articles by Topic
Biological Sciences
Featured Portals
Articles by Topic
Edited by Eli Yablonovitch, University of California, Berkeley, CA, and approved August 31, 2015 (received for review June 22, 2015)
Significance
Arthropod biophotonic nanostructures provide a plethora of complex geometries. Although the variety of geometric forms observed reflects those found in amphiphilic self-assembly, the biological formation principles are more complex. This paper addresses the chiral single gyroid in the Green Hairstreak butterfly Callophrys rubi, robustly showing that the formation process produces both the left- and right-handed enantiomers but with distinctly different likelihood. An interpretation excludes the molecular chirality of chitin as the determining feature of the enantiomeric type, emphasizing the need to identify other chirality-specific factors within the membrane-based biological formation model. These findings contribute to an understanding of nature’s ability to control secondary features of the structure formation, such as enantiomeric type and crystallographic texture, informing bioinspired self-assembly strategies.
Abstract
The wing scales of the Green Hairstreak butterfly Callophrys rubi consist of crystalline domains with sizes of a few micrometers, which exhibit a congenitally handed porous chitin microstructure identified as the chiral triply periodic single-gyroid structure. Here, the chirality and crystallographic texture of these domains are investigated by means of electron tomography. The tomograms unambiguously reveal the coexistence of the two enantiomeric forms of opposite handedness: the left- and right-handed gyroids. These two enantiomers appear with nonequal probabilities, implying that molecularly chiral constituents of the biological formation process presumably invoke a chiral symmetry break, resulting in a preferred enantiomeric form of the gyroid structure. Assuming validity of the formation model proposed by Ghiradella H (1989) J Morphol 202(1):69–88 and Saranathan V, et al. (2010) Proc Natl Acad Sci USA 107(26):11676–11681, where the two enantiomeric labyrinthine domains of the gyroid are connected to the extracellular and intra-SER spaces, our findings imply that the structural chirality of the single gyroid is, however, not caused by the molecular chirality of chitin. Furthermore, the wing scales are found to be highly textured, with a substantial fraction of domains exhibiting the <001> directions of the gyroid crystal aligned parallel to the scale surface normal. Both findings are needed to completely understand the photonic purpose of the single gyroid in gyroid-forming butterflies. More importantly, they show the level of control that morphogenesis exerts over secondary features of biological nanostructures, such as chirality or crystallographic texture, providing inspiration for biomimetic replication strategies for synthetic self-assembly mechanisms.
Footnotes
- ↵1To whom correspondence should be addressed. Email: erdmann.spiecker{at}fau.de.
Author contributions: B.W., B.B., G.E.S.-T., K.M., and E.S. designed research; B.W., B.B., and C.D. performed research; B.W., B.B., G.E.S.-T., and E.S. analyzed data; and B.W., B.B., G.E.S.-T., and E.S. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1511354112/-/DCSupplemental.
Coexistence of both gyroid chiralities in C. rubi
Sign up for Article Alerts
Jump to section
You May Also be Interested in
Several large or long-lived animals seem strangely resistant to developing cancer. Elucidating the reasons why could lead to promising cancer-fighting strategies in humans.
Image credit: Shutterstock.com/ronnybas frimages.
PNAS Profile of NAS member and biochemist Hao Wu
A study suggests a putative gene-expression hallmark common to monogamous male vertebrates of some species, namely cichlid fishes, dendrobatid frogs, passeroid songbirds, common voles, and deer mice, and identifies 24 candidate genes potentially associated with monogamy.
Image courtesy of Yusan Yang (University of Pittsburgh, Pittsburgh).
Physical and social well-being in old age are linked to self-assessments of life worth, and a spectrum of behavioral, economic, health, and social variables may influence whether aging individuals believe they are leading meaningful lives.
Image courtesy of Pixabay/MabelAmber.