Lineage-specific diversification in the usage of D-glutamate and D-aspartate in early-branching metazoans

Abstract

D-amino acids are unique and essential signaling molecules in neural, hormonal, and immune systems. However, the presence of D-amino acids and their recruitment in early animals is mostly unknown due to limited information about prebilaterian metazoans. Here, we performed the comparative survey of L-/D-aspartate and L-/D-glutamate in representatives of four phyla of basal Metazoa: cnidarians (Aglantha); placozoans (Trichoplax), sponges (Sycon) and ctenophores (Pleurobrachia, Mnemiopsis, Bolinopsis, and Beroe), which are descendants of ancestral animal lineages distinct from Bilateria. Specifically, we used high-performance capillary electrophoresis for microchemical assays and quantification of the enantiomers. L-glutamate and L-aspartate were abundant analytes in all species studied. However, we showed that the placozoans, cnidarians, and sponges had high micromolar concentrations of D-aspartate, whereas D-glutamate was not detectable. In contrast, we found that in ctenophores, D-glutamate was the dominant enantiomer with no or trace amounts of D-aspartate. This situation illuminates prominent lineage-specific diversifications in the recruitment of D-amino acids and suggests distinct signaling functions of these molecules early in the animal evolution. We also hypothesize that a deep ancestry of such recruitment events might provide some constraints underlying the evolution of neural and other signaling systems in Metazoa. Highlights• D-amino acids are essential for intercellular signaling and evolution • Enantiomers have been quantified in early-branching animals • Lineage-specific recruitment of D-glutamate could occur in ctenophores • D-aspartate is one of the primary enantiomers in other metazoans • Deep ancestry of such events could provide constraints in the evolution of signaling Graphical Abstract:Graphical abstract: D-amino acids are essential for intercellular signaling. Direct microchemical quantification of enantiomers in representatives of earlybranching animals suggests lineagespecific recruitments of D-glutamate and D-aspartate. Deep ancestry of such events might provide some constraints underlying the evolution of neural and other signaling systems in Metazoa.

Nitric oxide signaling in ctenophores

“…Unique NIT (PF08376) domains (Oulavallickal et al, 2017), containing cyclases, were previously identified in Trichoplax (Moroz et al, 2020) as candidates for nitrite/nitrate sensors, similar to bacteria (Shu et al, 2003;Camargo et al, 2007). Mnemiopsis has one sequence (ML02033a) associated with the same cluster (Figure 5) but with a highly derived NIT-like region and unknown function.…”

“…This tree confirms a highly derived nature of NOS in ctenophores, probably reflecting their accelerated evolution and a possible bottleneck in their paleontological history around the Permian extinction (Whelan et al, 2017). The tree also highlights several independent radiation events with duplication and triplication of NOSs in lineages leading to placozoans, cnidarians, and vertebrates [see also (Moroz et al, 2020)]. However, representative species from both Porifera and Ctenophora have only one NOS gene.…”

“…As a result, they are crucial to reconstruct the evolution and overall architecture of animal signaling pathways, including NO-dependent transmission. Yet only several papers deal with NO biology in Cnidaria and Porifera; and one publication discusses NO synthesis in placozoans (Moroz et al, 2020).…”

Expanding of Life Strategies in Placozoa: Insights From Long-Term Culturing of Trichoplax and Hoilungia

“…Chemoattractant/repellents can be signaling molecules from microorganisms or other cell types. Symbiont-host signaling can include changes in nitric oxide gradients (Moroz et al, 2020b) or regional differences in amino acid composition, interconversion of D-and L-forms (Moroz et al, 2020a), the formation of oxygen radicals, which are toxic to bacteria, etc.…”