Microbial community structure and functional traits involved in the adaptation of culturable bacteria within the gut of amphipods from the deepest ocean

Microbiol Spectr. 2024 Dec 10:e0072324. doi: 10.1128/spectrum.00723-24. Online ahead of print.

Abstract

The Hadal Zone is acknowledged for its extreme environmental conditions, especially high hydrostatic pressures. The dominant scavengers in the Hadal Zone, Hadal amphipods, fulfill vital roles in the Hadal food web and ecological niches. However, research on the gut microbiota of amphipods related to ecological functions and environmental adaptation is still limited. Here, we used 16S rRNA sequencing technology and a culture-dependent method to analyze the composition of the gut microbiota in Amphipoda living in the Mariana Trench. A total of 16 bacterial genera were identified. Among them, Firmicutes and Proteobacteria were the predominant phyla. The adaptability of gut probiotics to the environment was investigated. Pediococcus pentosaceus XY62 was picked up as the representative strain to elucidate the ecological functions of gut microbes in amphipods. The ProBio database and the K-B agar diffusion method indicated that P. pentosaceus XY62 exhibited the highest probiotic activity compared with all other isolated strains. Specific metabolic pathways and transporter systems that contribute to a range of environmental adaptation strategies have been revealed by genomic analysis of P. pentosaceus XY62. The environmental response genes and a specialized KDP transport system allow it to adapt to the challenging conditions of the Hadal Zone. In addition, the presence of antibacterial compounds and antibiotic resistance genes, as well as the ability to form a biofilm, facilitated the successful colonization of P. pentosaceus XY62 in the gut environment.

Importance: Amphipods are widely distributed in the Hadal trenches, and the study of their gut microbes has garnered considerable scientific interest. Our research breaks away from traditional omics approaches, innovatively combining sequencing technologies with culture-dependent methods to analyze the gut microbiome structure of amphipods from the Mariana Trench. This not only complements the current omics-dominated field but also paves the way for future resource development of extreme microbes. Furthermore, by conducting genomic analyses and functional validations on a representative strain, we have uncovered its probiotic effects and strategies for adapting to extreme environments. This provides new insights into the theoretical study of the ecological functions of deep-sea bacteria. Overall, our findings offer a fresh perspective on the microbial community structure and environmental adaptation strategies of gut microorganisms in the Hadal Zone.

Keywords: Mariana Trench; amphipods; environmental adaptation; genome; gut microbes.