Frequent Occurrence and Metabolic Versatility of Marinifilaceae Bacteria as Key Players in Organic Matter Mineralization in Global Deep Seas

ABSTRACT Transfer of animal and plant detritus of both terrestrial and marine origins to the deep sea occurs on a global scale. Microorganisms play an important role in mineralizing them therein, but these are yet to be identified in situ. To observe key bacteria involved, we conducted long-term in...

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Main Authors: Jianyang Li, Chunming Dong, Qiliang Lai, Guangyi Wang, Zongze Shao
Format: Article
Language:English
Published: American Society for Microbiology 2022-12-01
Series:mSystems
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/msystems.00864-22
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author Jianyang Li
Chunming Dong
Qiliang Lai
Guangyi Wang
Zongze Shao
author_facet Jianyang Li
Chunming Dong
Qiliang Lai
Guangyi Wang
Zongze Shao
author_sort Jianyang Li
collection DOAJ
description ABSTRACT Transfer of animal and plant detritus of both terrestrial and marine origins to the deep sea occurs on a global scale. Microorganisms play an important role in mineralizing them therein, but these are yet to be identified in situ. To observe key bacteria involved, we conducted long-term in situ incubation and found that members of the family Marinifilaceae (MF) occurred as some of the most predominant bacteria thriving on the new inputs of plant and animal biomasses in the deep sea in both marginal and oceanic areas. This taxon is diverse and ubiquitous in marine environments. A total of 11 MAGs belonging to MF were retrieved from metagenomic data and diverged into four subgroups in the phylogenomic tree. Based on metagenomic and metatranscriptomic analyses, we described the metabolic features and in situ metabolizing activities of different subgroups. The MF-2 subgroup, which dominates plant detritus-enriched cultures, specializes in polysaccharide degradation and lignin oxidation and has high transcriptional activities of related genes in situ. Intriguingly, members of this subgroup encode a nitrogen fixation pathway to compensate for the shortage of nitrogen sources inside the plant detritus. In contrast, other subgroups dominating the animal tissue-supported microbiomes are distinguished from MF-2 with regard to carbon and nitrogen metabolism and exhibit high transcriptional activity for proteolysis in situ. Despite these metabolic divergences of MF lineages, they show high in situ transcriptional activities for organic fermentation and anaerobic respiration (reductions of metal and/or dimethyl sulfoxide). These results highlight the role of previously unrecognized Marinifilaceae bacteria in organic matter mineralization in marine environments by coupling carbon and nitrogen cycling with metal and sulfur. IMPORTANCE Microbial mineralization of organic matter has a significant impact on the global biogeochemical cycle. This report confirms the role of Marinifilaceae in organic degradation in the oceans, with a contribution to ocean carbon cycling that has previously been underestimated. It was the dominant taxon thriving on plant and animal biomasses in our in situ incubator, as well as in whale falls and wood falls. At least 9 subgroups were revealed, and they were widely distributed in oceans globally but predominant in organic-matter-rich environments, with an average relative abundance of 8.3%. Different subgroups display a preference for the degradation of different macromolecules (polysaccharides, lignin, and protein) and adapt to their environments via special metabolic mechanisms.
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spelling doaj.art-ce85a409d46542d092b412df208f87202022-12-22T04:23:55ZengAmerican Society for MicrobiologymSystems2379-50772022-12-017610.1128/msystems.00864-22Frequent Occurrence and Metabolic Versatility of Marinifilaceae Bacteria as Key Players in Organic Matter Mineralization in Global Deep SeasJianyang Li0Chunming Dong1Qiliang Lai2Guangyi Wang3Zongze Shao4Key Laboratory of Marine Genetic Resources, Third Institute of Oceanography, Ministry of Natural Resources of PR China, Xiamen, People’s Republic of ChinaKey Laboratory of Marine Genetic Resources, Third Institute of Oceanography, Ministry of Natural Resources of PR China, Xiamen, People’s Republic of ChinaKey Laboratory of Marine Genetic Resources, Third Institute of Oceanography, Ministry of Natural Resources of PR China, Xiamen, People’s Republic of ChinaSchool of Environmental Science and Engineering, Tianjin University, Tianjin, People’s Republic of ChinaKey Laboratory of Marine Genetic Resources, Third Institute of Oceanography, Ministry of Natural Resources of PR China, Xiamen, People’s Republic of ChinaABSTRACT Transfer of animal and plant detritus of both terrestrial and marine origins to the deep sea occurs on a global scale. Microorganisms play an important role in mineralizing them therein, but these are yet to be identified in situ. To observe key bacteria involved, we conducted long-term in situ incubation and found that members of the family Marinifilaceae (MF) occurred as some of the most predominant bacteria thriving on the new inputs of plant and animal biomasses in the deep sea in both marginal and oceanic areas. This taxon is diverse and ubiquitous in marine environments. A total of 11 MAGs belonging to MF were retrieved from metagenomic data and diverged into four subgroups in the phylogenomic tree. Based on metagenomic and metatranscriptomic analyses, we described the metabolic features and in situ metabolizing activities of different subgroups. The MF-2 subgroup, which dominates plant detritus-enriched cultures, specializes in polysaccharide degradation and lignin oxidation and has high transcriptional activities of related genes in situ. Intriguingly, members of this subgroup encode a nitrogen fixation pathway to compensate for the shortage of nitrogen sources inside the plant detritus. In contrast, other subgroups dominating the animal tissue-supported microbiomes are distinguished from MF-2 with regard to carbon and nitrogen metabolism and exhibit high transcriptional activity for proteolysis in situ. Despite these metabolic divergences of MF lineages, they show high in situ transcriptional activities for organic fermentation and anaerobic respiration (reductions of metal and/or dimethyl sulfoxide). These results highlight the role of previously unrecognized Marinifilaceae bacteria in organic matter mineralization in marine environments by coupling carbon and nitrogen cycling with metal and sulfur. IMPORTANCE Microbial mineralization of organic matter has a significant impact on the global biogeochemical cycle. This report confirms the role of Marinifilaceae in organic degradation in the oceans, with a contribution to ocean carbon cycling that has previously been underestimated. It was the dominant taxon thriving on plant and animal biomasses in our in situ incubator, as well as in whale falls and wood falls. At least 9 subgroups were revealed, and they were widely distributed in oceans globally but predominant in organic-matter-rich environments, with an average relative abundance of 8.3%. Different subgroups display a preference for the degradation of different macromolecules (polysaccharides, lignin, and protein) and adapt to their environments via special metabolic mechanisms.https://journals.asm.org/doi/10.1128/msystems.00864-22deep seaMarinifilaceaebiodiversityorganic matter mineralizationlignin oxidationnitrogen fixation
spellingShingle Jianyang Li
Chunming Dong
Qiliang Lai
Guangyi Wang
Zongze Shao
Frequent Occurrence and Metabolic Versatility of Marinifilaceae Bacteria as Key Players in Organic Matter Mineralization in Global Deep Seas
mSystems
deep sea
Marinifilaceae
biodiversity
organic matter mineralization
lignin oxidation
nitrogen fixation
title Frequent Occurrence and Metabolic Versatility of Marinifilaceae Bacteria as Key Players in Organic Matter Mineralization in Global Deep Seas
title_full Frequent Occurrence and Metabolic Versatility of Marinifilaceae Bacteria as Key Players in Organic Matter Mineralization in Global Deep Seas
title_fullStr Frequent Occurrence and Metabolic Versatility of Marinifilaceae Bacteria as Key Players in Organic Matter Mineralization in Global Deep Seas
title_full_unstemmed Frequent Occurrence and Metabolic Versatility of Marinifilaceae Bacteria as Key Players in Organic Matter Mineralization in Global Deep Seas
title_short Frequent Occurrence and Metabolic Versatility of Marinifilaceae Bacteria as Key Players in Organic Matter Mineralization in Global Deep Seas
title_sort frequent occurrence and metabolic versatility of marinifilaceae bacteria as key players in organic matter mineralization in global deep seas
topic deep sea
Marinifilaceae
biodiversity
organic matter mineralization
lignin oxidation
nitrogen fixation
url https://journals.asm.org/doi/10.1128/msystems.00864-22
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