Catecholic Compounds in Ctenophore Colloblast and Nerve Net Proteins Suggest a Structural Role for DOPA-Like Molecules in an Early-Diverging Animal Lineage

Biol Bull. 2019 Feb;236(1):55-65. doi: 10.1086/700695. Epub 2018 Dec 10.

Abstract

Ctenophores, or comb jellies, are among the earliest-diverging extant animal lineages. Several recent phylogenomic studies suggest that they may even be the sister group to all other animals. This unexpected finding remains difficult to contextualize, particularly given ctenophores' unique and sometimes poorly understood physiology. Colloblasts, a ctenophore-specific cell type found on the surface of these animals' tentacles, are emblematic of this difficulty. The exterior of the colloblast is dotted with granules that burst and release an adhesive on contact with prey, ensnaring it for consumption. To date, little is known about the fast-acting underwater adhesive that these cells secrete or its biochemistry. We present evidence that proteins in the colloblasts of the ctenophore Pleurobrachia bachei incorporate catecholic compounds similar to the amino acid l-3,4-dihydroxyphenylalanine. These compounds are associated with adhesive-containing granules on the surface of colloblasts, suggesting that they may play a role in prey capture, akin to dihydroxyphenylalanine-based adhesives in mussel byssus. We also present unexpected evidence of similar catecholic compounds in association with the subepithelial nerve net. There, catecholic compounds are present in spatial patterns similar to those of l-3,4-dihydroxyphenylalanine and its derivatives in cnidarian nerves, where they are associated with membranes and possess unknown functionality. This "structural" use of catecholic molecules in ctenophores represents the earliest-diverging animal lineage in which this trait has been observed, though it remains unclear whether structural catechols are deeply rooted in animals or whether they have arisen multiple times.

Keywords: -DOPA, -3,4-dihydroxyphenylalanine; -diphenols, -diphenols; AcOH, acetic acid; CTAB, cetrimonium bromide; DOPA, dihydroxyphenylalanine; FIF, formaldehyde-induced fluorescence; PBS, phosphate-buffered saline; PFA, paraformaldehyde; TCA, tricholoracetic acid..

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Biological Evolution
  • Catechols / metabolism*
  • Ctenophora / chemistry*
  • Ctenophora / metabolism*
  • Dihydroxyphenylalanine / chemistry
  • Dihydroxyphenylalanine / metabolism*
  • Nerve Net / chemistry
  • Proteins / chemistry*

Substances

  • Catechols
  • Proteins
  • Dihydroxyphenylalanine