Convergent evolution of signal-structure interfaces for maintaining symbioses

Abstract

Symbiotic microbes are essential to the ecological success and evolutionary diversification of multicellular organisms. The establishment and stability of bipartite symbioses are shaped by mechanisms ensuring partner fidelity between host and symbiont. In this minireview, we demonstrate how the interface of chemical signals and host structures influences fidelity between legume root nodules and rhizobia, Hawaiian bobtail squid light organs and Allivibrio fischeri, and fungus-growing ant crypts and Pseudonocardia. Subsequently, we illustrate the morphological diversity and widespread phylogenetic distribution of specialized structures used by hosts to house microbial symbionts, indicating the importance of signal-structure interfaces across the history of multicellular life. These observations, and the insights garnered from well-studied bipartite associations, demonstrate the need to concentrate on the signal-structure interface in complex and multipartite systems, including the human microbiome.

Figure 1.. Signal-structure interfaces in bipartite associations between (A) legumes and rhizobia, (B) Hawaiian bobtail squid and A. fischeri, and (C) attine ants and Pseudonocardia.

The arrows indicate the direction of signals from producer to respondent and are arranged from top to bottom in each panel to indicate the order of signaling. FLV, flavonoids; NF, nodulation factors; NCR, nodule-specific cysteine-rich peptides; PG, peptidoglycan; OMVs; outer membrane vesicles; TCT, tracheal cytotoxin; NO, nitric oxide. Image credits: legume, rhizobia, and root nodule, Jean Michel Ané; bobtail squid, Mark Mandell; A. fischeri from [28]; light organ from Spencer Nyholm, under the terms of the Creative Commons Attribution License; attine ant, Ted Schultz; Pseudonocardia, Cameron Currie; ant crypt, Cameron Currie.

Figure 2.. Convergent evolution of structures to maintain microbial symbionts across the eukaryotic tree of life.

The phylogenetic tree shows the relationships between different eukaryotic lineages. Each inset represents an example of a eukaryotic host (left) from the specified lineage that uses a specialized structure (right) to establish and maintain a bipartite association with a microbial symbiont. Image credits: flashlight fish, Stefan Herlitze; flashlight fish light organ adapted from [69] under the terms of the Creative Commons Attribution License; ship worm and gill, Margo Haygood; bobtail squid and light organ, Mark Mandel; southern pine beetle, Erich Vallery under the terms of the Creative Commons Attribution License; mycangia, Kier Klepzig [70]; attine ant, Don Parsons; ant crypt, Cameron Currie; nematode and vesicle modified from [71] under the terms of the Creative Commons Attribution License; legume and root nodule, Jean Michel Ané.