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UniProt release 2017_10

Published October 25, 2017

Headline

Of smell and social life

Ants are arguably the greatest success story in the history of terrestrial metazoa. On average, ants constitute 15-20% of the terrestrial animal biomass. All the ~ 12,000 known ant species are eusocial, i.e. they have a sophisticated collective behavior characterized by a division of labor that creates groups, sometimes called castes, specialized in tasks such as reproduction, brood care and foraging . Individuals of one caste usually lose the ability to perform at least one behavior characteristic of individuals in another caste. It is thought that ant sociality depends on their sense of smell. Indeed while the Drosophila melanogaster genome contains about 69 odorant receptor (Or) genes, ant genomes have undergone a dramatic expansion with close to 350 Ors, representing one of the largest yet known repertoires of Ors among insects. Other chemosensory receptor genes, such as gustatory receptors and ionotropic glutamate receptors, have not undergone a similar expansion. Ors are expressed by Or neurons, which project axons to the antennal lobe, a region analogous to the olfactory bulb in vertebrates. The antennal lobe consists of numerous globule-shaped neuropils known as glomeruli, where initial synaptic integration occurs before olfactory information is sent to the central brain. Here again a drastic amplification occurred. Close to 450 glomeruli have been identified in the Camponotus floridanus ant versus only 42 in Drosophila. These observations are consistent with a crucial role for odorant perception in the complex chemical communication in ants, but so far there has no genetic confirmation of this hypothesis.

In insects, Ors dimerize with a highly conserved 7-transmembrane protein called Orco (Odorant Receptor COreceptor) and form ligand-gated ion channels that activate Or neurons upon odorant binding. Orco knockout in fruit flies, locusts, mosquitoes, and moths impairs responses to odorants. An Orco knockout in ants would allow testing of the hypothesis that the expanded Or repertoire is required for chemical communication. However social insects are especially hard to genetically modify, the eggs of ants are very sensitive and difficult to raise without workers, and the life cycle is complicated and drawn out, making it difficult to obtain large quantities of genetically modified offspring in a reasonable time frame.
In spite of these difficulties, 2 teams managed to successfully knockout Orco using CRISPR/Cas9 technology, providing the scientific community with the first genetically modified ants. This achievement was made possible through tenacity and a smart choice of the ant species. Yan et al. worked on Harpegnathos saltator ants. This species shows a remarkable reproductive plasticity: in the absence of a queen or when a worker is completely isolated, non-reproductive workers can become reproductive pseudoqueens (or gamergaters). It is thought that this transition is induced by the lack of queen pheromones which normally would repress it. When isolated, unmated gamergaters lay unfertilized eggs that develop into haploid males. Taking advantage of the gamergate transition, Yan et al. generated hemizygous mutant males. The transgenic males were identified by forewing genotyping. They did not exhibit any overt phenotype and were fully fertile. They could be crossed to receptive females to produce heterozygous and homozygous mutant females. Identification of transgenic females was more complicated. Females have no wings and could be genotyped only after being sacrified. All experiments were therefore done blindly. This denotes a rare enthusiasm for science that merits being emphasized!

Trible et al. chose Ooceraea biroi, a very distantly related species, as it diverged some 100 million years ago from H. saltator. Unlike most other ant species, O. biroi reproduces via parthenogenesis, so stable germ-line modifications can be obtained from the clonal progeny of injected individuals without laboratory crosses.

Both groups observed consistent phenotypes. The response to general odorants was reduced. Mutant insects wandered out of the social group and were unable to forage successfully. They did not produce progeny because they laid very few eggs and did not care for their brood. They appeared to be largely unable to communicate with conspecifics. Unexpectedly they exhibited a dramatic decrease in the size of the antennal lobes, as well as in the number of glomeruli. The remaining glomeruli tended to be bigger than in wild-type ants. The reason for this neuro-anatomical phenotype is unclear at this stage. However these results confirm the central role of olfaction in eusocial behavior.

As of this release, freshly annotated Harpegnathos saltator and Ooceraea biroi Orco entries are available in UniProtKB/Swiss-Prot.

Changes to the controlled vocabulary of human diseases

New diseases:

Modified disease:

Changes to the controlled vocabulary for PTMs

New terms for the feature key ‘Cross-link’ (‘CROSSLNK’ in the flat file):

  • Cyclopeptide (Gly-Arg)
  • Cyclopeptide (Ser-Lys)

New term for the feature key ‘Lipidation’ (‘LIPID’ in the flat file):

  • S-palmitoleoyl cysteine

New terms for the feature key ‘Modified residue’ (‘MOD_RES’ in the flat file):

  • ADP-ribosyl glutamic acid
  • N6-(2-hydroxyisobutyryl)lysine
  • N6-butyryllysine
  • N6-poly(beta-hydroxybutyryl)lysine
  • N6-propionyllysine
  • O3-poly(beta-hydroxybutyryl)serine
  • S-poly(beta-hydroxybutyryl)cysteine
Modified terms for the feature key ‘Modified residue’ (‘MOD_RES’ in the flat file):
  • N6-poly(methylaminopropyl)lysine > N6(beta-hydroxybutyryl)lysine
  • O-palmitoleyl serine -> O-palmitoleoyl serine

Changes to keywords

New keyword:

Modified keyword: