Genomics of Marine and Aquatic Bacteria: A Focus on Novel Taxa, Diversity and Biotechnological Potential

A special issue of Microorganisms (ISSN 2076-2607). This special issue belongs to the section "Environmental Microbiology".

Deadline for manuscript submissions: closed (15 August 2023) | Viewed by 11157

Special Issue Editors


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Guest Editor
G. B. Elyakov Pacific Institute of Bioorganic Chemistry Far Eastern Branch of Russian Academy of Sciences, Vladivostok, Russian
Interests: marine bacteria; diversity; phylogeny; novel taxa; bioactive metabolite

E-Mail Website
Guest Editor
G.B. Elyakov Pacific Institute of Bioorganic Chemistry, Far Eastern Branch, Russian Academy of Sciences, 690022 Vladivostok, Russia
Interests: genomics; phylogeny; biochemistry; genome bioprospecting
Special Issues, Collections and Topics in MDPI journals

E-Mail Website
Guest Editor
G.B. Elyakov Pacific Institute of Bioorganic Chemistry, Far Eastern Branch, Russian Academy of Sciences, Vladivostok, Russian
Interests: marine bacteria; diversity; phylogeny; novel taxa

Special Issue Information

Dear Colleagues,

Marine and aquatic bacteria represent an enormous amount of biodiversity and are a valuable source for bioprospecting aims such as the search of novel bioactive compounds, functional foods ingredients, and polymers. Our knowledge regarding the bacterial world has been greatly advanced by exploring bacterial genome sequences, especially in bacterial systematics, genetic diversity, and microbial evolution. Advances in genomics promote the application of genetic information of bacteria in virtually unlimited areas. To describe new taxa, environmental microbiologists nowadays have to combine culture-dependent studies with genome sequence analyses. The research of bacteria recovered from underexplored, remote, and extreme environments, such as arctic seas, the deep-sea, or underground waters and sediments, is a challenge for the understanding of microbial diversity, its conservation, and further biotechnological use. We firmly believe that new taxa will result in new genes, new knowledge, and new opportunities.

Dr. Lyudmila A. Romanenko
Dr. Marina P. Isaeva
Dr. Valeriya Kurilenko
Guest Editors

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Keywords

  • bacteria
  • diversity
  • bacterial communities
  • novel taxa
  • phylogeny
  • genome analysis
  • marine and aquatic environments

Published Papers (10 papers)

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21 pages, 4110 KiB  
Article
LPS-Dephosphorylating Cobetia amphilecti Alkaline Phosphatase of PhoA Family Divergent from the Multiple Homologues of Cobetia spp.
by Larissa Balabanova, Svetlana Bakholdina, Nina Buinovskaya, Yulia Noskova, Oksana Kolpakova, Vanessa Vlasova, Georgii Bondarev, Aleksandra Seitkalieva, Oksana Son and Liudmila Tekutyeva
Microorganisms 2024, 12(3), 631; https://doi.org/10.3390/microorganisms12030631 - 21 Mar 2024
Viewed by 956
Abstract
A highly active alkaline phosphatase (ALP) of the protein structural family PhoA, from a mussel gut-associated strain of the marine bacterium Cobetia amphilecti KMM 296 (CmAP), was found to effectively dephosphorylate lipopolysaccharides (LPS). Therefore, the aim of this work was to perform a [...] Read more.
A highly active alkaline phosphatase (ALP) of the protein structural family PhoA, from a mussel gut-associated strain of the marine bacterium Cobetia amphilecti KMM 296 (CmAP), was found to effectively dephosphorylate lipopolysaccharides (LPS). Therefore, the aim of this work was to perform a comprehensive bioinformatics analysis of the structure, and to suggest the physiological role of this enzyme in marine bacteria of the genus Cobetia. A scrutiny of the CmAP-like sequences in 36 available Cobetia genomes revealed nine homologues intrinsic to the subspecies C. amphilecti, whereas PhoA of a distant relative Cobetia crustatorum JO1T carried an inactive mutation. However, phylogenetic analysis of all available Cobetia ALP sequences showed that each strain of the genus Cobetia possesses several ALP variants, mostly the genes encoding for PhoD and PhoX families. The C. amphilecti strains have a complete set of four ALP families’ genes, namely: PhoA, PafA, PhoX, and two PhoD structures. The Cobetia marina species is distinguished by the presence of only three PhoX and PhoD genes. The Cobetia PhoA proteins are clustered together with the human and squid LPS-detoxifying enzymes. In addition, the predicted PhoA biosynthesis gene cluster suggests its involvement in the control of cellular redox balance, homeostasis, and cell cycle. Apparently, the variety of ALPs in Cobetia spp. indicates significant adaptability to phosphorus-replete and depleted environments and a notable organophosphate destructor in eco-niches from which they once emerged, including Zostera spp. The ALP clusterization and degree of similarity of the genus-specific biosynthetic genes encoding for ectoine and polyketide cluster T1PKS, responsible for sulfated extracellular polysaccharide synthesis, coincide with a new whole genome-based taxonomic classification of the genus Cobetia. The Cobetia strains and their ALPs are suggested to be adaptable for use in agriculture, biotechnology and biomedicine. Full article
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11 pages, 4570 KiB  
Article
tilS and rpoB: New Molecular Markers for Phylogenetic and Biodiversity Studies of the Genus Thiothrix
by Nikolai V. Ravin, Dmitry D. Smolyakov, Nikita D. Markov, Alexey V. Beletsky, Andrey V. Mardanov, Tatyana S. Rudenko and Margarita Yu. Grabovich
Microorganisms 2023, 11(10), 2521; https://doi.org/10.3390/microorganisms11102521 - 9 Oct 2023
Viewed by 891
Abstract
Currently, the phylogeny of the genus Thiothrix is based on comparative whole genome analysis because of the high homology of the 16S ribosomal RNA gene sequences within the genus. We analyzed the possibility of using various conservative genes as phylogenetic markers for the [...] Read more.
Currently, the phylogeny of the genus Thiothrix is based on comparative whole genome analysis because of the high homology of the 16S ribosomal RNA gene sequences within the genus. We analyzed the possibility of using various conservative genes as phylogenetic markers for the genus Thiothrix. We found that the levels of similarity of the nucleotide sequences of the tRNA(Ile)-lysidine synthase (tilS) and the β subunit of RNA polymerase (rpoB) genes are in good agreement with the average nucleotide identity (ANI) values between the genomes of various representatives of the genus Thiothrix. The genomes of Thiothrix strains MK1, WS, DNT52, DNT53, and H33 were sequenced. Taxonomic analysis using both whole genomes and the tilS gene consistently showed that MK1 and WS belong to Thiothrix lacustris, while DNT52, DNT53, and H33 belong to Thiothrix subterranea. The tilS gene fragments were subjected to high-throughput sequencing to profile the Thiothrix mat of a sulfidic spring, which revealed the presence of known species of Thiothrix and new species-level phylotypes. Thus, the use of tilS and rpoB as phylogenetic markers will allow for rapid analyses of pure cultures and natural communities for the purpose of phylogenetic identification of representatives of the genus Thiothrix. Full article
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13 pages, 3306 KiB  
Article
Description of Aequorivita aurantiaca sp. nov. Isolated from Coastal Sediment, and Comparative Genomic Analysis and Biogeographic Distribution of the Genus Aequorivita
by Jun-Cheng Liu, Yu-Qi Ye, Xin-Yun Tan, Zong-Jun Du and Meng-Qi Ye
Microorganisms 2023, 11(10), 2518; https://doi.org/10.3390/microorganisms11102518 - 9 Oct 2023
Viewed by 975
Abstract
A novel Gram-stain-negative, facultatively anaerobic, and non-motile bacterial strain, designated SDUM287046T, was isolated from the coastal sediments of Jingzi Port of Weihai, China. Cells of strain SDUM287046T were rod-shaped with widths of 0.4–0.5 μm and lengths of 0.7–1.4 μm and [...] Read more.
A novel Gram-stain-negative, facultatively anaerobic, and non-motile bacterial strain, designated SDUM287046T, was isolated from the coastal sediments of Jingzi Port of Weihai, China. Cells of strain SDUM287046T were rod-shaped with widths of 0.4–0.5 μm and lengths of 0.7–1.4 μm and could produce flexirubin-type pigments. Optimum growth of strain SDUM287046T occurred at 33–35 °C, pH 7.0, and with 2% (w/v) NaCl. Oxidase activity was negative, but catalase activity was positive. Phylogenetic analysis based on 16S rRNA gene sequence revealed that strain SDUM287046T was most closely related to Aequorivita aquimaris D-24T (98.3%). The main cellular fatty acids were iso-C15:0, anteiso-C15:0, iso-C17:0 3–OH, and summed feature 9 (comprised of iso-C17:1 ω9c and/or C16:0 10-methyl). The sole respiratory quinone was MK-6. The polar lipids consisted of phosphatidylethanolamine (PE), one aminolipid (AL), three unidentified glycolipids (GL), and three unidentified lipids (L). The DNA G + C content was 39.3 mol%. According to the integrated results of phylogenetic, physiological, biochemical, and chemotaxonomic characteristics, we propose that strain SDUM287046T represents a novel species of the genus Aequorivita, for which the name Aequorivita aurantiaca sp. nov. is proposed. The type strain is SDUM287046T (=KCTC 92754T = MCCC 1H01418T). Comparative genomic analysis showed that the 16 Aequorivita species shared 1453 core genes and differed mainly in amino acid metabolism, cofactor metabolism, and vitamin metabolism. Biogeographic distribution analysis indicated that the marine environments were the primary habitat of Aequorivita bacteria. Full article
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17 pages, 3716 KiB  
Article
Characterization and Genomic Analysis of Fererhizobium litorale gen. nov., sp. nov., Isolated from the Sandy Sediments of the Sea of Japan Seashore
by Lyudmila Romanenko, Nadezhda Otstavnykh, Naoto Tanaka, Valeriya Kurilenko, Vasily Svetashev, Liudmila Tekutyeva, Valery Mikhailov and Marina Isaeva
Microorganisms 2023, 11(10), 2385; https://doi.org/10.3390/microorganisms11102385 - 25 Sep 2023
Cited by 2 | Viewed by 963
Abstract
The taxonomic status of two gram-negative, whitish-pigmented motile bacteria KMM 9576T and KMM 9553 isolated from a sandy sediment sample from the Sea of Japan seashore was defined. Phylogenetic analysis revealed that strains KMM 9576T and KMM 9553 represent a distinct [...] Read more.
The taxonomic status of two gram-negative, whitish-pigmented motile bacteria KMM 9576T and KMM 9553 isolated from a sandy sediment sample from the Sea of Japan seashore was defined. Phylogenetic analysis revealed that strains KMM 9576T and KMM 9553 represent a distinct lineage within the family Rhizobiaceae, sharing 100% 16S rRNA sequence similarity and 99.5% average nucleotide identity (ANI) to each other. The strains showed the highest 16S rRNA sequence similarities of 97.4% to Sinorhizobium garamanticum LMG 24692T, 96.9% to Ensifer adhaerens NBRC 100388T, and 96.8% to Pararhizobium giardinii NBRC 107135T. The ANI values between strain KMM 9576T and Ensifer adhaerens NBRC 100388T, Sinorhizobium fredii USDA 205T, Pararhizobium giardinii NBRC 107135T, and Rhizobium leguminosarum NBRC 14778T were 79.9%, 79.6%, 79.4%, and 79.2%, respectively. The highest core-proteome average amino acid identity (cpAAI) values of 82.1% and 83.1% were estimated between strain KMM 9576T and Rhizobium leguminosarum NBRC 14778T and ‘Rhizobium album’ NS-104, respectively. The DNA GC contents were calculated from a genome sequence to be 61.5% (KMM 9576T) and 61.4% (KMM 9553). Both strains contained the major ubiquinone Q-10 and C18:1ω7c as the dominant fatty acid followed by 11-methyl C18:1ω7c and C19:0 cyclo, and polar lipids consisted of phosphatidylcholine, phosphatidylethanolamine, phosphatidylglycerol, an unidentified aminophospholipid, and two unidentified phospholipids. Based on phylogenetic and phylogenomic analyses, and phenotypic characterization, strains KMM 9576T and KMM 9553 are concluded to represent a novel genus and species, for which the name Fererhizobium litorale gen. nov., sp. nov. is proposed. The type strain of the type species is strain KMM 9576T (=NRIC 0957T). Full article
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20 pages, 6265 KiB  
Article
Genome Analysis and Potential Ecological Functions of Members of the Genus Ensifer from Subsurface Environments and Description of Ensifer oleiphilus sp. nov.
by Alexey P. Ershov, Tamara L. Babich, Denis S. Grouzdev, Diyana S. Sokolova, Ekaterina M. Semenova, Alexander N. Avtukh, Andrey B. Poltaraus, Elena A. Ianutsevich and Tamara N. Nazina
Microorganisms 2023, 11(9), 2314; https://doi.org/10.3390/microorganisms11092314 - 14 Sep 2023
Cited by 1 | Viewed by 979
Abstract
The current work deals with genomic analysis, possible ecological functions, and biotechnological potential of two bacterial strains, HO-A22T and SHC 2-14, isolated from unique subsurface environments, the Cheremukhovskoe oil field (Tatarstan, Russia) and nitrate- and radionuclide-contaminated groundwater (Tomsk region, Russia), respectively. New [...] Read more.
The current work deals with genomic analysis, possible ecological functions, and biotechnological potential of two bacterial strains, HO-A22T and SHC 2-14, isolated from unique subsurface environments, the Cheremukhovskoe oil field (Tatarstan, Russia) and nitrate- and radionuclide-contaminated groundwater (Tomsk region, Russia), respectively. New isolates were characterized using polyphasic taxonomy approaches and genomic analysis. The genomes of the strains HO-A22T and SHC 2-14 contain the genes involved in nitrate reduction, hydrocarbon degradation, extracellular polysaccharide synthesis, and heavy metal detoxification, confirming the potential for their application in various environmental biotechnologies. Genomic data were confirmed by cultivation studies. Both strains were found to be neutrophilic, chemoorganotrophic, facultatively anaerobic bacteria, growing at 15–33 °C and 0–1.6% NaCl (w/v). The 16S rRNA gene sequences of the strains were similar to those of the type strains of the genus Ensifer (99.0–100.0%). Nevertheless, genomic characteristics of strain HO-A22T were below the thresholds for species delineation: the calculated average nucleotide identity (ANI) values were 83.7–92.4% (<95%), and digital DNA–DNA hybridization (dDDH) values were within the range of 25.4–45.9% (<70%), which supported our conclusion that HO-A22T (=VKM B-3646T = KCTC 92427T) represented a novel species of the genus Ensifer, with the proposed name Ensifer oleiphilus sp. nov. Strain SHC 2-14 was assigned to the species ‘Ensifer canadensis’, which has not been validly published. This study expanded the knowledge about the phenotypic diversity among members of the genus Ensifer and its potential for the biotechnologies of oil recovery and radionuclide pollution treatment. Full article
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14 pages, 3236 KiB  
Article
Growing in Saltwater: Biotechnological Potential of Novel Methylotuvimicrobium- and Methylomarinum-like Methanotrophic Bacteria
by Ekaterina N. Tikhonova, Ruslan Z. Suleimanov, Igor Y. Oshkin, Aleksey A. Konopkin, Diana V. Fedoruk, Nikolai V. Pimenov and Svetlana N. Dedysh
Microorganisms 2023, 11(9), 2257; https://doi.org/10.3390/microorganisms11092257 - 8 Sep 2023
Viewed by 1011
Abstract
Methanotrophic bacteria that possess a unique ability of using methane as a sole source of carbon and energy have attracted considerable attention as potential producers of a single-cell protein. So far, this biotechnology implied using freshwater methanotrophs, although many regions of the world [...] Read more.
Methanotrophic bacteria that possess a unique ability of using methane as a sole source of carbon and energy have attracted considerable attention as potential producers of a single-cell protein. So far, this biotechnology implied using freshwater methanotrophs, although many regions of the world have limited freshwater resources. This study aimed at searching for novel methanotrophs capable of fast growth in saltwater comparable in composition with seawater. A methane-oxidizing microbial consortium containing Methylomarinum- and Methylotuvimicrobium-like methanotrophs was enriched from sediment from the river Chernavka (water pH 7.5, total salt content 30 g L−1), a tributary river of the hypersaline Lake Elton, southern Russia. This microbial consortium, designated Ch1, demonstrated stable growth on natural gas in a bioreactor in media with a total salt content of 23 to 35.9 g L−1 at a dilution rate of 0.19–0.21 h−1. The highest biomass yield of 5.8 g cell dry weight (CDW)/L with a protein content of 63% was obtained during continuous cultivation of the consortium Ch1 in a medium with a total salt content of 29 g L−1. Isolation attempts resulted in obtaining a pure culture of methanotrophic bacteria, strain Ch1-1. The 16S rRNA gene sequence of strain Ch1-1 displayed 97.09–97.24% similarity to the corresponding gene fragments of characterized representatives of Methylomarinum vadi, methanotrophs isolated from marine habitats. The genome of strain Ch1-1 was 4.8 Mb in size and encoded 3 rRNA operons, and about 4400 proteins. The genome contained the gene cluster coding for ectoine biosynthesis, which explains the ability of strain Ch1-1 to tolerate high salt concentration. Full article
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21 pages, 3080 KiB  
Article
Chitinolytic and Fungicidal Potential of the Marine Bacterial Strains Habituating Pacific Ocean Regions
by Iuliia Pentekhina, Olga Nedashkovskaya, Aleksandra Seitkalieva, Vladimir Gorbach, Lubov Slepchenko, Natalya Kirichuk, Anna Podvolotskaya, Oksana Son, Liudmila Tekutyeva and Larissa Balabanova
Microorganisms 2023, 11(9), 2255; https://doi.org/10.3390/microorganisms11092255 - 8 Sep 2023
Viewed by 1061
Abstract
Screening for chitinolytic activity in the bacterial strains from different Pacific Ocean regions revealed that the highly active representatives belong to the genera Microbulbifer, Vibrio, Aquimarina, and Pseudoalteromonas. The widely distributed chitinolytic species was Microbulbifer isolated from the sea [...] Read more.
Screening for chitinolytic activity in the bacterial strains from different Pacific Ocean regions revealed that the highly active representatives belong to the genera Microbulbifer, Vibrio, Aquimarina, and Pseudoalteromonas. The widely distributed chitinolytic species was Microbulbifer isolated from the sea urchin Strongylocentrotus intermedius. Among seventeen isolates with confirmed chitinolytic activity, only the type strain P. flavipulchra KMM 3630T and the strains of putatively new species Pseudoalteromonas sp. B530 and Vibrio sp. Sgm 5, isolated from sea water (Vietnam mollusc farm) and the sea urchin S. intermedius (Peter the Great Gulf, the Sea of Japan), significantly suppressed the hyphal growth of Aspergillus niger that is perspective for the biocontrol agents’ development. The results on chitinolytic activities and whole-genome sequencing of the strains under study, including agarolytic type strain Z. galactanivorans DjiT, found the new functionally active chitinase structures and biotechnological potential. Full article
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12 pages, 12874 KiB  
Article
Zwartia vadi sp. nov., a Novel Species of the GKS98 Cluster Isolated from a Stream, and the Reclassification of ‘Achromobacter Panacis’ as Zwartia panacis comb. nov
by Miri S. Park, Ilnam Kang and Jang-Cheon Cho
Microorganisms 2023, 11(9), 2150; https://doi.org/10.3390/microorganisms11092150 - 24 Aug 2023
Viewed by 777
Abstract
A Gram-stain-negative, aerobic, motile by gliding, and rod-shaped bacterium, designated IMCC34845T, was isolated from a freshwater stream in the Republic of Korea. The results of 16S rRNA gene-based phylogenetic analyses showed that strain IMCC34845T was affiliated with the genus Zwartia [...] Read more.
A Gram-stain-negative, aerobic, motile by gliding, and rod-shaped bacterium, designated IMCC34845T, was isolated from a freshwater stream in the Republic of Korea. The results of 16S rRNA gene-based phylogenetic analyses showed that strain IMCC34845T was affiliated with the genus Zwartia and was most closely related to ‘Achromobacter panacis’ DCY105T (100%) and Zwartia hollandica LF4-65T (98.9%). The whole-genome sequence of strain IMCC34845T was 3.2 Mbp in size with a 51.5% DNA G+C content. The average nucleotide identity (ANI) and digital DNA-DNA hybridization (dDDH) values between strain IMCC34845T and ‘Achromobacter panacis’ KCTC 42751T were 77.7% and 20.7%, respectively, revealing that they are independent species. Moreover, the strains IMCC34845T and KCTC 42751T exhibited ≤ 72.5% ANI and ≤18.5% dDDH values with closely related species Zwartia hollandica LF4-65T, further supporting that the two strains represent each novel species of the genus. The major respiratory quinone of strain IMCC34845T was ubiquinone-8 (Q-8), and the predominant cellular fatty acids were C16:0 (41.3%) and C17:0 cyclo (34.5%). The major polar lipids of the strain were diphosphatidylglycerol, phosphatidylglycerol, phosphatidylethanolamine, unidentified phospholipids, and unidentified aminolipids. Based on the phylogenetic, genomic, physiological, and chemotaxonomic characteristics, strain IMCC34845T was considered to represent a novel species within the genus Zwartia, for which the name Zwartia vadi sp. nov. is proposed. The type of strain is IMCC34845T (=KCTC 92920T = NBRC 114902T). Furthermore, based on the taxonomic data, ‘Achromobacter panacis’ is proposed to be reclassified as Zwartia panacis comb. nov. Full article
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14 pages, 1744 KiB  
Article
Metagenomic Analyses Reveal the Influence of Depth Layers on Marine Biodiversity on Tropical and Subtropical Regions
by Bianca C. F. Santiago, Iara D. de Souza, João Vitor F. Cavalcante, Diego A. A. Morais, Mikaelly B. da Silva, Matheus Augusto de B. Pasquali and Rodrigo J. S. Dalmolin
Microorganisms 2023, 11(7), 1668; https://doi.org/10.3390/microorganisms11071668 - 27 Jun 2023
Cited by 3 | Viewed by 1511
Abstract
The emergence of open ocean global-scale studies provided important information about the genomics of oceanic microbial communities. Metagenomic analyses shed light on the structure of marine habitats, unraveling the biodiversity of different water masses. Many biological and environmental factors can contribute to marine [...] Read more.
The emergence of open ocean global-scale studies provided important information about the genomics of oceanic microbial communities. Metagenomic analyses shed light on the structure of marine habitats, unraveling the biodiversity of different water masses. Many biological and environmental factors can contribute to marine organism composition, such as depth. However, much remains unknown about microbial communities’ taxonomic and functional features in different water layer depths. Here, we performed a metagenomic analysis of 76 publicly available samples from the Tara Ocean Project, distributed in 8 collection stations located in tropical or subtropical regions, and sampled from three layers of depth (surface water layer—SRF, deep chlorophyll maximum layer—DCM, and mesopelagic zone—MES). The SRF and DCM depth layers are similar in abundance and diversity, while the MES layer presents greater diversity than the other layers. Diversity clustering analysis shows differences regarding the taxonomic content of samples. At the domain level, bacteria prevail in most samples, and the MES layer presents the highest proportion of archaea among all samples. Taken together, our results indicate that the depth layer influences microbial sample composition and diversity. Full article
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10 pages, 4224 KiB  
Brief Report
Genomics of Yoonia sp. Isolates (Family Roseobacteraceae) from Lake Zhangnai on the Tibetan Plateau
by Xiaoyuan Feng and Peng Xing
Microorganisms 2023, 11(11), 2817; https://doi.org/10.3390/microorganisms11112817 - 20 Nov 2023
Viewed by 763
Abstract
Understanding the genomic differentiation between marine and non-marine aquatic microbes remains a compelling question in ecology. While previous research has identified several lacustrine lineages within the predominantly marine Roseobacteraceae family, limited genomic data have constrained our understanding of their ecological adaptation mechanisms. In [...] Read more.
Understanding the genomic differentiation between marine and non-marine aquatic microbes remains a compelling question in ecology. While previous research has identified several lacustrine lineages within the predominantly marine Roseobacteraceae family, limited genomic data have constrained our understanding of their ecological adaptation mechanisms. In this study, we isolated four novel Yoonia strains from a brackish lake on the Tibetan Plateau. These strains have diverged from their marine counterparts within the same genus, indicating a recent habitat transition event from marine to non-marine environments. Metabolic comparisons and ancestral genomic reconstructions in a phylogenetic framework reveal metabolic shifts in salinity adaptation, compound transport, aromatics degradation, DNA repair, and restriction systems. These findings not only corroborate the metabolic changes commonly observed in other non-marine Roseobacters but also unveil unique adaptations, likely reflecting the localized metabolic changes in responses to Tibetan Plateau environments. Collectively, our study expands the known genomic diversity of non-marine Roseobacteraceae lineages and enhances our understanding of microbial adaptations to lacustrine ecosystems. Full article
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