Genome Reduction in <italic toggle="yes">Psychromonas</italic> Species within the Gut of an Amphipod from the Ocean’s Deepest Point

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 individu...

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Autores principales: Weipeng Zhang, Ren-Mao Tian, Jin Sun, Salim Bougouffa, Wei Ding, Lin Cai, Yi Lan, Haoya Tong, Yongxin Li, Alan J. Jamieson, Vladimir B. Bajic, Jeffrey C. Drazen, Douglas Bartlett, Pei-Yuan Qian
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Publicado: American Society for Microbiology 2018
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spelling oai:doaj.org-article:aba88eb7d6524d87883450e8b2a7c7c92021-12-02T18:15:44ZGenome Reduction in <italic toggle="yes">Psychromonas</italic> Species within the Gut of an Amphipod from the Ocean’s Deepest Point10.1128/mSystems.00009-182379-5077https://doaj.org/article/aba88eb7d6524d87883450e8b2a7c7c92018-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00009-18https://doaj.org/toc/2379-5077ABSTRACT 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.Weipeng ZhangRen-Mao TianJin SunSalim BougouffaWei DingLin CaiYi LanHaoya TongYongxin LiAlan J. JamiesonVladimir B. BajicJeffrey C. DrazenDouglas BartlettPei-Yuan QianAmerican Society for Microbiologyarticleamphipodgut microbiotaMariana TrenchPsychromonasMicrobiologyQR1-502ENmSystems, Vol 3, Iss 3 (2018)
institution DOAJ
collection DOAJ
language EN
topic amphipod
gut microbiota
Mariana Trench
Psychromonas
Microbiology
QR1-502
spellingShingle amphipod
gut microbiota
Mariana Trench
Psychromonas
Microbiology
QR1-502
Weipeng Zhang
Ren-Mao Tian
Jin Sun
Salim Bougouffa
Wei Ding
Lin Cai
Yi Lan
Haoya Tong
Yongxin Li
Alan J. Jamieson
Vladimir B. Bajic
Jeffrey C. Drazen
Douglas Bartlett
Pei-Yuan Qian
Genome Reduction in <italic toggle="yes">Psychromonas</italic> Species within the Gut of an Amphipod from the Ocean’s Deepest Point
description 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.
format article
author Weipeng Zhang
Ren-Mao Tian
Jin Sun
Salim Bougouffa
Wei Ding
Lin Cai
Yi Lan
Haoya Tong
Yongxin Li
Alan J. Jamieson
Vladimir B. Bajic
Jeffrey C. Drazen
Douglas Bartlett
Pei-Yuan Qian
author_facet Weipeng Zhang
Ren-Mao Tian
Jin Sun
Salim Bougouffa
Wei Ding
Lin Cai
Yi Lan
Haoya Tong
Yongxin Li
Alan J. Jamieson
Vladimir B. Bajic
Jeffrey C. Drazen
Douglas Bartlett
Pei-Yuan Qian
author_sort Weipeng Zhang
title Genome Reduction in <italic toggle="yes">Psychromonas</italic> Species within the Gut of an Amphipod from the Ocean’s Deepest Point
title_short Genome Reduction in <italic toggle="yes">Psychromonas</italic> Species within the Gut of an Amphipod from the Ocean’s Deepest Point
title_full Genome Reduction in <italic toggle="yes">Psychromonas</italic> Species within the Gut of an Amphipod from the Ocean’s Deepest Point
title_fullStr Genome Reduction in <italic toggle="yes">Psychromonas</italic> Species within the Gut of an Amphipod from the Ocean’s Deepest Point
title_full_unstemmed Genome Reduction in <italic toggle="yes">Psychromonas</italic> Species within the Gut of an Amphipod from the Ocean’s Deepest Point
title_sort genome reduction in <italic toggle="yes">psychromonas</italic> species within the gut of an amphipod from the ocean’s deepest point
publisher American Society for Microbiology
publishDate 2018
url https://doaj.org/article/aba88eb7d6524d87883450e8b2a7c7c9
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