Codependence in the Nephromyces species swarm depends on heterospecific bacterial endosymbionts

Abstract

The phylum Apicomplexa encompasses 6000 ubiquitous animal parasites, including Plasmodium, the most deadly human parasite on Earth. Anciently parasitic lineages, like apicomplexans, lose core metabolic pathways over time, as they evolve less costly scavenging mechanisms. The recent description of a mutualistic apicomplexan, Nephromyces, from deep within this parasitic group, opened the possibility of an evolutionary innovation that allowed an escape from a parasitic lifestyle. Nuclear genome data from Nephromyces, as well as the three bacterial symbionts that live within this species complex, demonstrate that the bacteria within Nephromyces contribute essential cofactors and amino acids that have enabled Nephromyces to abandon a parasitic lifestyle. Among these, bacterial lipoic acid appears to be a key cofactor for the reduction of virulence in Nephromyces. However, whereas we use FISH microscopy to reveal that each individual Nephromyces harbors no more than one endosymbiont type, no single bacterial endosymbiont can account for all missing metabolites. Based on the unique habitat of Nephromyces, as well as genomic, culturing, and wild population data, we conclude that Nephromyces has evolved as an extraordinary clade of codependent species, unlike any previously described.