SoxY gene family expansion underpins adaptation to diverse hosts and environments in symbiotic sulfide oxidizers

Abstract

ABSTRACT Sulfur-oxidizing bacteria (SOB) have developed distinct ecological strategies to obtain reduced sulfur compounds for growth. These range from specialists that can only use a limited range of reduced sulfur compounds to generalists that can use many different forms as electron donors. Forming intimate symbioses with animal hosts is another highly successful ecological strategy for SOB, as animals, through their behavior and physiology, can enable access to sulfur compounds. Symbioses have evolved multiple times in a range of animal hosts and from several lineages of SOB. They have successfully colonized a wide range of habitats, from seagrass beds to hydrothermal vents, with varying availability of symbiont energy sources. Our extensive analyses of sulfur transformation pathways in 234 genomes of symbiotic and free-living SOB revealed widespread conservation in metabolic pathways for sulfur oxidation in symbionts from different host species and environments, raising the question of how they have adapted to such a wide range of distinct habitats. We discovered a gene family expansion of soxY in these genomes, with up to five distinct copies per genome. Symbionts harboring only the “canonical” soxY were typically ecological “specialists” that are associated with specific host subfamilies or environments (e.g., hydrothermal vents, mangroves). Conversely, symbionts with multiple divergent soxY genes formed versatile associations across diverse hosts in various marine environments. We hypothesize that expansion and diversification of the soxY gene family could be one genomic mechanism supporting the metabolic flexibility of symbiotic SOB enabling them and their hosts to thrive in a range of different and dynamic environments. IMPORTANCE Sulfur metabolism is thought to be one of the most ancient mechanisms for energy generation in microorganisms. A diverse range of microorganisms today rely on sulfur oxidation for their metabolism. They can be free-living, or they can live in symbiosis with animal hosts, where they power entire ecosystems in the absence of light, such as in the deep sea. In the millions of years since they evolved, sulfur-oxidizing bacteria have adopted several highly successful strategies; some are ecological “specialists,” and some are “generalists,” but which genetic features underpin these ecological strategies are not well understood. We discovered a gene family that has become expanded in those species that also seem to be “generalists,” revealing that duplication, repurposing, and reshuffling existing genes can be a powerful mechanism driving ecological lifestyle shifts.