Genome Reduction in Psychromonas Species within the Gut of an Amphipod from the Ocean's Deepest Point.

Weipeng Zhang,Lin Cai,Haoya Tong,Douglas Bartlett,Wei Ding,Yongxin Li,Yi Lan,Ren-Mao Tian,Jeffrey C Drazen,Pei-Yuan Qian,Vladimir B Bajic,Alan J Jamieson,Jin Sun,Salim Bougouffa

doi:10.1128/msystems.00009-18

Abstract

Amphipods are the dominant scavenging metazoan species in the Mariana Trench, the deepest known point in Earth's oceans. Here the gut microbiota of the amphipod Hirondellea gigas collected from the Challenger and Sirena Deeps of the Mariana Trench were investigated. The 11 amphipod individuals included for analyses were dominated by Psychromonas, of which a nearly complete genome was successfully recovered (designated CDP1). Compared with previously reported free-living Psychromonas strains, CDP1 has a highly reduced genome. Genome alignment showed deletion of the trimethylamine N-oxide (TMAO) reducing gene cluster in CDP1, suggesting that the "piezolyte" function of TMAO is more important than its function in respiration, which may lead to TMAO accumulation. In terms of nutrient utilization, the bacterium retains its central carbohydrate metabolism but lacks most of the extended carbohydrate utilization pathways, suggesting the confinement of Psychromonas to the host gut and sequestration from more variable environmental conditions. Moreover, CDP1 contains a complete formate hydrogenlyase complex, which might be involved in energy production. The genomic analyses imply that CDP1 may have developed adaptive strategies for a lifestyle within the gut of the hadal amphipod H.gigas. IMPORTANCE As a unique but poorly investigated habitat within marine ecosystems, hadal trenches have received interest in recent years. This study explores the gut microbial composition and function in hadal amphipods, which are among the dominant carrion feeders in hadal habitats. Further analyses of a dominant strain revealed genomic features that may contribute to its adaptation to the amphipod gut environment. Our findings provide new insights into animal-associated bacteria in the hadal biosphere.

Highlights

Amphipods are the dominant scavenging metazoan species in the Mariana Trench, the deepest known point in Earth’s oceans
The “Candidatus Hepatoplasma,” Burkholderia, and Methanosarcina bacteria identified in this study have been reported to be symbionts of terrestrial isopods [30], bean bugs [31], and termites [32], respectively
The presence of these microbial groups points to a specific association between the gut microbiota and the H. gigas host

Summary

Introduction

Amphipods are the dominant scavenging metazoan species in the Mariana Trench, the deepest known point in Earth’s oceans. The gut microbiota of the amphipod Hirondellea gigas collected from the Challenger and Sirena Deeps of the Mariana Trench were investigated. The genomic analyses imply that CDP1 may have developed adaptive strategies for a lifestyle within the gut of the hadal amphipod H. gigas. Further analyses of a dominant strain revealed genomic features that may contribute to its adaptation to the amphipod gut environment. The animal gut microbiota has been shown to be involved in a number of aspects of normal host physiology, such as nutritional status and environmental adaptation [7,8,9,10,11], and the environment of the host can affect the gut microbial composition. In a study on two euryhaline species, Oreochromis niloticus (Nile tilapia) and Litopenaeus vannamei (Pacific white shrimp), the change in salinity is linked to the shift in the gut microbial composition, possibly because of the salinity stress response of the host and subsequent stress exerted on the associated microbes [11]

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Results

Conclusion