The identification of the new species Nitratireductor thuwali sp. nov. reveals the untapped diversity of hydrocarbon-degrading culturable bacteria from the arid mangrove sediments of the Red Sea
IntroductionThe geological isolation, lack of freshwater inputs and specific internal water circulations make the Red Sea one of the most extreme—and unique—oceans on the planet. Its high temperature, salinity and oligotrophy, along with the consistent input of hydrocarbons due to its geology (e.g.,...
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| Format: | Article |
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Frontiers Media S.A.
2023-05-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2023.1155381/full |
| _version_ | 1797835664528506880 |
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| author | Ramona Marasco Grégoire Michoud Fatmah O. Sefrji Marco Fusi Chakkiath P. Antony Kholoud A. Seferji Alan Barozzi Giuseppe Merlino Daniele Daffonchio |
| author_facet | Ramona Marasco Grégoire Michoud Fatmah O. Sefrji Marco Fusi Chakkiath P. Antony Kholoud A. Seferji Alan Barozzi Giuseppe Merlino Daniele Daffonchio |
| author_sort | Ramona Marasco |
| collection | DOAJ |
| description | IntroductionThe geological isolation, lack of freshwater inputs and specific internal water circulations make the Red Sea one of the most extreme—and unique—oceans on the planet. Its high temperature, salinity and oligotrophy, along with the consistent input of hydrocarbons due to its geology (e.g., deep-sea vents) and high oil tankers traffic, create the conditions that can drive and influence the assembly of unique marine (micro)biomes that evolved to cope with these multiple stressors. We hypothesize that mangrove sediments, as a model-specific marine environment of the Red Sea, act as microbial hotspots/reservoirs of such diversity not yet explored and described.MethodsTo test our hypothesis, we combined oligotrophic media to mimic the Red Sea conditions and hydrocarbons as C-source (i.e., crude oil) with long incubation time to allow the cultivation of slow-growing environmentally (rare or uncommon) relevant bacteria.Results and discussionThis approach reveals the vast diversity of taxonomically novel microbial hydrocarbon degraders within a collection of a few hundred isolates. Among these isolates, we characterized a novel species, Nitratireductor thuwali sp. nov., namely, Nit1536T. It is an aerobic, heterotrophic, Gram-stain-negative bacterium with optimum growth at 37°C, 8 pH and 4% NaCl, whose genome and physiological analysis confirmed the adaptation to extreme and oligotrophic conditions of the Red Sea mangrove sediments. For instance, Nit1536T metabolizes different carbon substrates, including straight-chain alkanes and organic acids, and synthesizes compatible solutes to survive in salty mangrove sediments. Our results showed that the Red Sea represent a source of yet unknown novel hydrocarbon degraders adapted to extreme marine conditions, and their discovery and characterization deserve further effort to unlock their biotechnological potential. |
| first_indexed | 2024-04-09T14:56:07Z |
| format | Article |
| id | doaj.art-2ea303e613fb452e91b378eed5ca09c9 |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-04-09T14:56:07Z |
| publishDate | 2023-05-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-2ea303e613fb452e91b378eed5ca09c92023-05-02T04:40:29ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-05-011410.3389/fmicb.2023.11553811155381The identification of the new species Nitratireductor thuwali sp. nov. reveals the untapped diversity of hydrocarbon-degrading culturable bacteria from the arid mangrove sediments of the Red SeaRamona MarascoGrégoire MichoudFatmah O. SefrjiMarco FusiChakkiath P. AntonyKholoud A. SeferjiAlan BarozziGiuseppe MerlinoDaniele DaffonchioIntroductionThe geological isolation, lack of freshwater inputs and specific internal water circulations make the Red Sea one of the most extreme—and unique—oceans on the planet. Its high temperature, salinity and oligotrophy, along with the consistent input of hydrocarbons due to its geology (e.g., deep-sea vents) and high oil tankers traffic, create the conditions that can drive and influence the assembly of unique marine (micro)biomes that evolved to cope with these multiple stressors. We hypothesize that mangrove sediments, as a model-specific marine environment of the Red Sea, act as microbial hotspots/reservoirs of such diversity not yet explored and described.MethodsTo test our hypothesis, we combined oligotrophic media to mimic the Red Sea conditions and hydrocarbons as C-source (i.e., crude oil) with long incubation time to allow the cultivation of slow-growing environmentally (rare or uncommon) relevant bacteria.Results and discussionThis approach reveals the vast diversity of taxonomically novel microbial hydrocarbon degraders within a collection of a few hundred isolates. Among these isolates, we characterized a novel species, Nitratireductor thuwali sp. nov., namely, Nit1536T. It is an aerobic, heterotrophic, Gram-stain-negative bacterium with optimum growth at 37°C, 8 pH and 4% NaCl, whose genome and physiological analysis confirmed the adaptation to extreme and oligotrophic conditions of the Red Sea mangrove sediments. For instance, Nit1536T metabolizes different carbon substrates, including straight-chain alkanes and organic acids, and synthesizes compatible solutes to survive in salty mangrove sediments. Our results showed that the Red Sea represent a source of yet unknown novel hydrocarbon degraders adapted to extreme marine conditions, and their discovery and characterization deserve further effort to unlock their biotechnological potential.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1155381/fullheterotrophic bacteriacultivationmangrovesextreme adaptationrare biospherepetroleum hydrocarbon-degraders |
| spellingShingle | Ramona Marasco Grégoire Michoud Fatmah O. Sefrji Marco Fusi Chakkiath P. Antony Kholoud A. Seferji Alan Barozzi Giuseppe Merlino Daniele Daffonchio The identification of the new species Nitratireductor thuwali sp. nov. reveals the untapped diversity of hydrocarbon-degrading culturable bacteria from the arid mangrove sediments of the Red Sea Frontiers in Microbiology heterotrophic bacteria cultivation mangroves extreme adaptation rare biosphere petroleum hydrocarbon-degraders |
| title | The identification of the new species Nitratireductor thuwali sp. nov. reveals the untapped diversity of hydrocarbon-degrading culturable bacteria from the arid mangrove sediments of the Red Sea |
| title_full | The identification of the new species Nitratireductor thuwali sp. nov. reveals the untapped diversity of hydrocarbon-degrading culturable bacteria from the arid mangrove sediments of the Red Sea |
| title_fullStr | The identification of the new species Nitratireductor thuwali sp. nov. reveals the untapped diversity of hydrocarbon-degrading culturable bacteria from the arid mangrove sediments of the Red Sea |
| title_full_unstemmed | The identification of the new species Nitratireductor thuwali sp. nov. reveals the untapped diversity of hydrocarbon-degrading culturable bacteria from the arid mangrove sediments of the Red Sea |
| title_short | The identification of the new species Nitratireductor thuwali sp. nov. reveals the untapped diversity of hydrocarbon-degrading culturable bacteria from the arid mangrove sediments of the Red Sea |
| title_sort | identification of the new species nitratireductor thuwali sp nov reveals the untapped diversity of hydrocarbon degrading culturable bacteria from the arid mangrove sediments of the red sea |
| topic | heterotrophic bacteria cultivation mangroves extreme adaptation rare biosphere petroleum hydrocarbon-degraders |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2023.1155381/full |
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