Deep-sea Bacteroidetes from the Mariana Trench specialize in hemicellulose and pectin degradation typically associated with terrestrial systems

Zhu, Xiao-Yu, Li, Yang, Xue, Chun-Xu, Lidbury, Ian D. E. A., Todd, Jonathan D., Lea-Smith, David J. ORCID:, Tian, Jiwei, Zhang, Xiao-Hua and Liu, Jiwen (2023) Deep-sea Bacteroidetes from the Mariana Trench specialize in hemicellulose and pectin degradation typically associated with terrestrial systems. Microbiome, 11. ISSN 2049-2618

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Background: Hadal trenches (>6000 m) are the deepest oceanic regions on Earth and depocenters for organic materials. However, how these enigmatic microbial ecosystems are fueled is largely unknown, particularly the proportional importance of complex polysaccharides introduced through deposition from the photic surface waters above. In surface waters, Bacteroidetes are keystone taxa for the cycling of various algal-derived polysaccharides and the flux of carbon through the photic zone. However, their role in the hadal microbial loop is almost unknown. Results: Here, culture-dependent and culture-independent methods were used to study the potential of Bacteroidetes to catabolize diverse polysaccharides in Mariana Trench waters. Compared to surface waters, the bathypelagic (1000–4000 m) and hadal (6000–10,500 m) waters harbored distinct Bacteroidetes communities, with Mesoflavibacter being enriched at ≥ 4000 m and Bacteroides and Provotella being enriched at 10,400–10,500 m. Moreover, these deep-sea communities possessed distinct gene pools encoding for carbohydrate active enzymes (CAZymes), suggesting different polysaccharide sources are utilised in these two zones. Compared to surface counterparts, deep-sea Bacteroidetes showed significant enrichment of CAZyme genes frequently organized into polysaccharide utilization loci (PULs) targeting algal/plant cell wall polysaccharides (i.e., hemicellulose and pectin), that were previously considered an ecological trait associated with terrestrial Bacteroidetes only. Using a hadal Mesoflavibacter isolate (MTRN7), functional validation of this unique genetic potential was demonstrated. MTRN7 could utilize pectic arabinans, typically associated with land plants and phototrophic algae, as the carbon source under simulated deep-sea conditions. Interestingly, a PUL we demonstrate is likely horizontally acquired from coastal/land Bacteroidetes was activated during growth on arabinan and experimentally shown to encode enzymes that hydrolyze arabinan at depth. Conclusions: Our study implies that hadal Bacteroidetes exploit polysaccharides poorly utilized by surface populations via an expanded CAZyme gene pool. We propose that sinking cell wall debris produced in the photic zone can serve as an important carbon source for hadal heterotrophs and play a role in shaping their communities and metabolism. [MediaObject not available: see fulltext.].

Item Type: Article
Additional Information: Funding Information: This work was supported by the National Natural Science Foundation of China (no. 41976101, 92051115, and 92251303), the Laoshan Laboratory (no. LSKJ202203206), the Shandong Province Natural Science Foundation (ZR2022YQ38), the Fundamental Research Funds for the Central Universities (no. 202141009 and 202172002), and the Biotechnology and Biological Sciences Research Council, UK (BB/X005968), Natural Environmental Research Council, UK (NE/P012671, NE/S001352, NE/X000990, and NE/X014428 with DLS), and the Leverhulme trust (RPG-2020-413) grants in JDT’s lab.
Uncontrolled Keywords: bacteroidetes,cell wall polysaccharide utilization,hadal trench,metagenomics,sinking debris,microbiology,microbiology (medical),sdg 15 - life on land ,/dk/atira/pure/subjectarea/asjc/2400/2404
Faculty \ School: Faculty of Science > School of Biological Sciences
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Depositing User: LivePure Connector
Date Deposited: 26 Apr 2024 16:30
Last Modified: 30 Apr 2024 11:30
DOI: 10.1186/s40168-023-01618-7


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