Distinct microbial nitrogen cycling processes in the deepest part of the ocean

Author:

Huang Yuhan123ORCID,Zhang Xinxu12ORCID,Xin Yu4,Tian Jiwei5,Li Meng12ORCID

Affiliation:

1. Archaeal Biology Center, Shenzhen Key Laboratory of Marine Microbiome Engineering, Institute for Advanced Study, Shenzhen University, Shenzhen, China

2. Synthetic Biology Research Center, Institute for Advanced Study, Shenzhen University, Shenzhen, China

3. College of Life Sciences and Oceanography, Shenzhen University, Shenzhen, China

4. Key Laboratory of Marine Chemistry Theory and Technology, Ministry of Education, Institute for Advanced Ocean Study, Ocean University of China, Qingdao, Shandong, China

5. MOE Key Laboratory of Physical Oceanography, Frontiers Science Center for Deep Ocean Multispheres and Earth System, Ocean University of China, Qingdao, China

Abstract

ABSTRACT The Mariana Trench (MT) is the deepest part of the ocean on Earth. Previous studies have described the microbial community structures and functional potential in the seawater and surface sediment of MT. Still, the metabolic features and adaptation strategies of the microorganisms involved in nitrogen cycling processes are poorly understood. In this study, comparative metagenomic approaches were used to study microbial nitrogen cycling in three MT habitats, including hadal seawater [9,600–10,500 m below sea level (mbsl)], surface sediments [0–46 cm below seafloor (cmbsf) at a water depth between 7,143 and 8,638 mbsl], and deep sediments (200–306 cmbsf at a water depth of 8,300 mbsl). We identified five new nitrite-oxidizing bacteria (NOB) lineages that had adapted to the oligotrophic MT slope sediment, via their CO 2 fixation capability through the reductive tricarboxylic acid (rTCA) or Calvin-Benson-Bassham (CBB) cycle; an anammox bacterium might perform aerobic respiration and utilize sedimentary carbohydrates for energy generation because it contains genes encoding type A cytochrome c oxidase and complete glycolysis pathway. In seawater, abundant alkane-oxidizing Ketobacter species can fix inert N 2 released from other denitrifying and/or anammox bacteria. This study further expands our understanding of microbial life in the largely unexplored deepest part of the ocean. IMPORTANCE The metabolic features and adaptation strategies of the nitrogen cycling microorganisms in the deepest part of the ocean are largely unknown. This study revealed that anammox bacteria might perform aerobic respiration in response to nutrient limitation or O 2 fluctuations in the Mariana Trench sediments. Meanwhile, an abundant alkane-oxidizing Ketobacter species could fix N 2 in hadal seawater. This study provides new insights into the roles of hadal microorganisms in global nitrogen biogeochemical cycles. It substantially expands our understanding of the microbial life in the largely unexplored deepest part of the ocean.

Funder

MOST | National Natural Science Foundation of China

Guangdong Major Project of Basic and Applied Basic Research

Southern Marine Science and Engineering Guangdong Laboratory

Shenzhen University 2035 Program for Excellent Research

Synthetic Biology Research Center of Shenzhen University

Publisher

American Society for Microbiology

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