Genomic and metabolic insights into the first host-associated isolate of Psychrilyobacter.

Abstract

Although gut bacteria are vital to their hosts, few studies have focused on marine animals. Psychrilyobacter is frequently related to various marine animals, but its interaction with host remains unknown due to the lack of host-associated isolate or genomic information. Here, we combined cultivation-independent and cultivation-dependent methods to uncover the potential roles of Psychrilyobacter in the host abalone. The high-throughput sequencing and literature compiling results indicated that Psychrilyobacter is widely distributed in marine and terrestrial ecosystems with both host-associated and free-living lifestyles, but with a strong niche preference in the guts of marine invertebrates, especially abalone. By in vitro enrichment that mimicked the gut inner environment, the first host-related pure culture of Psychrilyobacter was isolated from the abalone intestine. Phylogenetic, physiological, and biochemical characterizations suggested that it represents a novel species named Psychrilyobacter haliotis B1. Carbohydrate utilization experiments and genomic evidence indicated that B1 can utilize diverse host-food-related monosaccharides and disaccharides but not polysaccharides, implying its potential role in the downstream fermentation instead of the upstream food degradation in the gut. Particularly, this strain showed potential to colonize the gut and benefit the host via different strategies, such as the short-chain fatty acids generation by fermenting peptides and/or amino acids, and the putative production of diverse vitamins and antibiotics to support the host growth and antipathogenicity. To our knowledge, strain B1 represents the first host-related pure culture of Psychrilyobacter; genomic and metabolic evidence showed some beneficial characteristics of the dominant gut anaerobe to the host. IMPORTANCE Psychrilyobacter is a globally distributed bacterial genus and with an inhabiting preference for guts of marine invertebrates. Due to the difficulty of cultivation and the limited genomic information, its role in host remains largely unknown. We isolated the first host-associated Psychrilyobacter species from abalone gut and uncovered its functional potential to the host through different mechanisms. Our findings provide some insights into the understanding of host-microbe interactions on a core taxon with the marine invertebrates, and the isolate may have an application potential in the protection of marine animals.