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ISSN : 1226-9999(Print)
ISSN : 2287-7851(Online)
Korean J. Environ. Biol. Vol.42 No.2 pp.143-157
DOI : https://doi.org/10.11626/KJEB.2024.42.2.143

A report on 29 unrecorded bacterial species isolated from the Nakdonggang River, Republic of Korea

Ahyoung Choi*, Ja Young Cho, Soo-Yeong Lee, Ji Young Jung, Kiwoon Baek, Seoni Hwang, Eui-Jin Kim, Jaeduk Goh
Biological Resources Research Department, Nakdonggang National Institute of Biological Resources (NNIBR), Sangju 37242, Republic of Korea
*Corresponding author Ahyoung Choi Tel. 054-530-0841 E-mail. aychoi@nnibr.re.kr

Contribution to Environmental Biology



▪ This study aims to offer a taxonomic perspective on species that have been reported abroad but have not yet been reported in Korea.


▪ To ensure that future researchers can access and preserve these biological resources, they have been deposited at FBCC (Freshwater Bioresources Culture Collection).


▪ This initiative will increase the availability of these resources for the scientific community, allowing for further research and exploration.


01/02/2024 15/04/2024 14/06/2024

Abstract


As part of the research program “Freshwater Prokaryotic Organisms Research and Discovery,” freshwater samples were collected from the Nakdonggang River. After plating the samples on several culture media and incubating aerobically, approximately 900 bacterial strains were isolated and identified using 16S rRNA gene sequences. Among the bacterial isolates showing higher than 98.7% 16S rRNA gene sequence similarity with those of already confirmed bacterial species previously unreported in Korea, 29 strains were selected. These strains were phylogenetically diverse and belonged to 3 phyla, 6 classes, 13 orders, and 21 genera. At the genus level, these previously unreported species were found to be affiliated with Novosphingobium, Sphingomonas, Polymorphobacter, Croceibacterium, Devosia, Endobacterium, Agaricicola, Bradyrhizobium, Paracoccus, and Pseudotabrizicola of the class Alphaproteobacteria; Undibacterium, Azonexus, and Dechloromonas of the class Betaproteobacteria; Acinetobacter and Budvicia of the class Gammaproteobacteria; Streptomyces, Nocardioides, Mycobacterium, and Cellulomonas of the phylum Actinomycetota; Flavobacterium and Pedobacter of the phylum Bacteroidota. These species were further characterized by examining their Gram reaction, colony and cell morphologies, biochemical properties, and phylogenetic positions. Detailed descriptions of these 29 previously unreported species are provided.


unrecorded bacterial species , freshwater , Nakdonggang River

초록

    1. INTRODUCTION

    In pursuit of bolstering national biological sovereignty, the Ministry of Environment has set forth the ambitious goal of securing 100,000 species of native organisms by 2030. As of 2024, the cataloging of 60,010 national biological species has been completed, encompassing the discovery of 5,039 prokaryotes, including bacteria, with this number steadily on the rise (NIBR 2023). Nevertheless, the emphasis on uncovering biological resources remains primarily directed towards marine and terrestrial environments, highlighting the imperative for a comprehensive investigation into the prokaryotic inhabitants of domestic freshwater environments.

    Freshwater environments, encompassing rivers, lakes, and groundwater, represent a mere 0.6% of Earth’s total water, excluding glaciers. Despite their limited proportion, they play a vital role in sustaining human life (Wetzel 2023). However, these environments are highly vulnerable to environmental degradation, particularly due to industrialization and climate change. Alarming statistics reveal an 84% decline in freshwater species since 1970 (WHO 2008). The distribution of species in freshwater environments varies depending on factors such as river systems, streams, lake habitats, seasonal variations, and water layers. Advances in in-depth sequencing technology have rapidly enhanced our understanding of bacterial diversity and the fundamental processes of microbial ecology. This has led to a deeper comprehension of the intricate relationship between the functioning of aquatic ecosystems and the formation of bacterial communities (Edwards et al. 2006;Huse et al. 2008).

    However, despite these technological advancements, the cultivation of predominant groups of microorganisms remains crucial for gaining a comprehensive understanding of bacteria and their ecological roles within freshwater environments. This cultivation-based approach provides valuable insights into the functional capabilities and interactions of these microbial communities in their natural habitats.

    Pseudomonadota is a bacterial phylum that underwent renaming from ‘Proteobacteria’ in 2021 (Oren and Garrity 2021). Presently, the phylum Pseudomonadota stands as the largest and most phenotypically diverse phylogenetic lineage. As of the time of this writing, taxonomic classification based on 16S rRNA gene sequences indicates that the phylum Pseudomonadota comprises six major phylogenetic classes: Acidithiobacillia, Alphaproteobacteria, Betaproteobacteria, Gammaproteobacteria, Hydrogenophilalia, and Zetaproteobacteria. Accounting for over 40% of all validly published prokaryotic genera, the Pseudomonadota encompass a significant portion of traditional Gram-negative bacteria (Stackebrandt et al. 1988). They exhibit remarkable metabolic diversity and hold substantial biological importance, encompassing the majority of known Gram-negative species of medical, veterinary, and industrial significance (Slonczewski et al. 2020).

    Actinomycetota is a bacterial phylum that underwent renaming from ‘Actinobacteria’ in 2021 (Oren and Garrity 2021). Representing a diverse phylum of Grampositive bacteria, the Actinomycetota are characterized by their high G+C content (Gao and Gupta 2012). They inhabit both terrestrial and aquatic environments and play a crucial role in various ecosystems (Servin et al. 2008). As of the time of this writing, taxonomic classification based on 16S rRNA gene sequences indicates that the phylum Actinomycetota comprises six classes: Acidimicrobiia, Actinomycetia, Coriobacteriia, Nitriliruptoria, Rubrobacteria, and Thermoleophilia. The Actinomycetota stands out as one of the dominant bacterial phyla, boasting one of the largest bacterial genera, Streptomyces. Streptomyces and other Actinomycetota play crucial roles in soil health by contributing significantly to biological buffering (Donald et al. 2022).

    Bacteroidota is a bacterial phylum that was renamed from ‘Bacteroidetes’ in 2021 (Oren and Garrity 2021). Comprising three large classes of Gram-negative, non-sporeforming, anaerobic or aerobic, and rodshaped bacteria, the phylum Bacteroidota is widely distributed in various environments, including soil, sediments, seawater, as well as in the gastrointestinal tract and on the skin of animals (Krieg et al. 2010). As of the time of writing, based on taxonomic classification using 16S rRNA gene sequences, there are six classes within the phylum Bacteroidota, including Bacteroidia, Chitinophagia, Cytophagia, Flavobacteriia, Saprospiria, and Sphingobacteriia.

    In this project, we collect physicochemical information and samples from various freshwater habitats, including rivers, wetlands, and brackish water areas, with a primary focus on the Nakdonggang River water system. The objective is to discover 29 previously unrecorded species by isolating prokaryotes from both river water and soil samples. Genetic information exceeding 1,350 base pairs is confirmed through 16S rRNA gene sequence analysis. To ensure taxonomic evidence, we gather transmission electron microscope image data, culture information (such as medium, temperature, and culture period), and information for polyphasic classification characteristic analysis. This report presents the phylogenetic and phenotypic characterization of these bacterial species.

    2. MATERIALS AND METHODS

    A total of 29 bacterial strains were isolated from the Nakdonggang River using the standard dilution plating method on several culture media, including marine agar 2211 (MA), 1/10-diluted MA (1/10 MA), Reasoner’s 2A (R2A), 1/10-diluted R2A (1/10 R2A), nutrient agar (NA), 1/10-diluted NA (1/10 NA), 1/10-diluted tryptic soy agar (1/10 TSA), or Inorganic Salts Starch (ISP) Agar 4. These isolates were subsequently incubated at 15-25°C for 14 days. Following serial dilution spreading, all strains were purified as single colonies, and the pure cultures were preserved as 20% glycerol suspensions at -80°C. The strain IDs, culture media, and incubation conditions are summarized in Table 1. Colony morphologies of the bacterial strains were observed on agar plates using a magnifying glass after the cells were cultivated until reaching the stationary phase. Cellular morphology and size were examined using transmission electron microscopy (Talos L120C; ThermoFisher Scientific, MA, USA). Gram staining was performed using a Gram-staining kit (BioMérieux, France), and biochemical characteristics were assessed using API 20NE galleries (BioMérieux, France) following the manufacturer’s instructions.

    For 16S rRNA sequence analysis, genomic DNA from the isolates was extracted using the DNeasy Blood & Tissue kit (Qiagen, Hilden, Germany) following the manufacturer’s instructions. The 16S rRNA gene of the strains was amplified by PCR using universal bacterial primers 27F and 1492R and sequenced via Sanger sequencing (Weisburg et al. 1991). The resulting almost full-length 16S rRNA gene sequences were identified using the “16S-based ID” service in EzBioCloud (Yoon et al. 2017), with a sequence similarity cutoff value set at 98.7%. Bacterial strains exhibiting ≥98.7% sequence similarity with known bacterial species previously unreported in Korea were selected as unreported bacterial species.

    For phylogenetic analyses, multiple sequence alignments between the 16S rRNA gene sequences of the isolates and those of reference-type strains were performed using the Clustal_W program and manually checked with EzEditor (Jeon et al. 2014). Based on the aligned sequences, phylogenetic trees were generated using the neighbor-joining method (Saitou and Nei 1987) with the Kimura 2-parameter model (Kimura 1980) implemented in MEGA 7.0 software (Kumar et al. 2016). The robustness of the inferred phylogenetic trees was evaluated through bootstrap analyses based on 1,000 random re-samplings (Felsenstein 1985).

    3. RESULTS AND DISCUSSION

    The 16S rRNA gene sequence analyses conducted on approximately 900 bacterial strains obtained in this study revealed that some strains belonged to novel species or species previously unreported in Korea. Among these, 29 strains exhibited ≥98.7% 16S rRNA gene sequence similarities with unrecorded bacterial species in Korea and belonged to 3 phyla, 6 classes, 13 orders, and 21 genera. The taxonomic composition and identification results of these species are summarized in Table 1. At the genus level, the unreported species were found to belong to various taxa, including Novosphingobium, Sphingomonas, Polymorphobacter, Croceibacterium, Devosia, Endobacterium, Agaricicola, Bradyrhizobium, Paracoccus, and Pseudotabrizicola within the class Alphaproteobacteria; Undibacterium, Azonexus, and Dechloromonas within the class Betaproteobacteria; Acinetobacter and Budvicia within the class Gammaproteobacteria; Streptomyces, Nocardioides, Mycobacterium, and Cellulomonas within the phylum Actinomycetota; Flavobacterium and Pedobacter within the phylum Bacteroidota. The phylogenetic tree of the bacterial strains assigned to the phylum Pseudomonadato is shown in Figure 1 and Figure 2, and the two phyla Actinomycetota and Bacteroidota are shown in Figure 3, respectively. These figures depict the phylogenetic relationships between the isolates and closely related species. Transmission electron microscopic images of the isolates are provided in Figure 4.

    In summary, this study identified 29 bacterial species previously unreported in Korean freshwater ecosystems, and the characteristics of these unreported bacterial species are presented and described herein.

    3.1. Description of Novosphingobium bradum 23ND15S-033

    Cells are Gram-stain-negative, non-flagellated, and rod-shaped. Colonies grown on R2A are circular, convex, and pale yellow after incubation for 7 days at 25°C. Positive for nitrate reduction, esculin hydrolysis, gelatinase, and β-galactosidase in API 20NE, but negative for indole production, glucose fermentation, arginine dihydrolase, and urease. D-glucose and D-mannose are utilized. Does not utilize L-arabinose, D-mannitol, N-acetyl-glucosamine, D-maltose, potassium gluconate, capric acid, adipic acid, malic acid, trisodium citrate, and phenylacetic acid. Strain 23ND15S-033 displays the highest 16S rRNA gene sequence similarity with Novosphingobium bradum STM-24T (99.1%). Strain 23ND15S-033 (=NNIBR2023641BA2573=FB CC-B15827) was isolated from riverside sediment collected in Ulju-gun, Ulsan, Korea (35°4ʹ13ʺN 128°8ʹ 2.9ʺE). The GenBank accession number of the 16S rRNA gene sequence is PP024214.

    3.2. Description of Novosphingobium silvae 23ND23W-034

    Cells are Gram-stain-negative, flagellated, and rodshaped. Colonies grown on MA are circular, convex, and ivory after incubation for 3 days at 20°C. Positive for esculin hydrolysis, and β-galactosidase in API 20NE, but negative for nitrate reduction, indole production, glucose fermentation, arginine dihydrolase, urease, and gelatinase. D-maltose, adipic acid, and malic acid are utilized. Does not utilize D-glucose, L-arabinose, D-mannose, D-mannitol, N-acetyl-glucosamine, potassium gluconate, capric acid, trisodium citrate, and phenylacetic acid. Strain 23ND23W-034 displays the highest 16S rRNA gene sequence similarity with Novosphingobium silvae FGD1T (99.9%). Strain 23ND23W- 034 (=NNIBR2023641BA456=FBCC-B13527) was isolated from surface water collected in Bonghwa-gun, Gyeongsangbuk-do (37°4ʹ0.7ʺN 128°59ʹ0.9ʺE). The GenBank accession number of the 16S rRNA gene sequence is PP024224.

    3.3. Description of Novosphingobium lubricantis 23ND49W-23

    Cells are Gram-stain-negative, non-flagellated, and rod-shaped. Colonies grown on 0.1 MA are circular, and pale yellow after incubation for 7 days at 25°C. Negative for nitrate reduction, indole production, glucose fermentation, arginine dihydrolase, urease, esculin hydrolysis, gelatinase, and β-galactosidase in API 20NE. Does not utilize D-glucose, L-arabinose, D-mannose, D-mannitol, N-acetyl-glucosamine, D-maltose, potassium gluconate, capric acid, adipic acid, malic acid, trisodium citrate, and phenylacetic acid. Strain 23ND49W-23 displays the highest 16S rRNA gene sequence similarity with Novosphingobium lubricantis KSS 165-70T (100.0%). Strain 23ND49W-23 (=NNIBR2023 641BA2569=FBCC-B15831) was isolated from surface water collected in Uljin-gun, Gyeongsangbuk-do, Korea (37°4ʹ24.57ʺN 129°23ʹ57.8ʺE). The GenBank accession number of the 16S rRNA gene sequence is OR999589.

    3.4. Description of Sphingomonas aracearum 23ND16S-022

    Cells are Gram-stain-negative, non-flagellated, and rod-shaped. Colonies grown on R2A are circular, convex, and yellow after incubation for 7 days at 25°C. Positive for esculin hydrolysis, gelatinase, and β-galactosidase in API 20NE, but negative for nitrate reduction, indole production, glucose fermentation, arginine dihydrolase, and urease. Does not utilize D-glucose, L-arabinose, D-mannose, D-mannitol, N-acetyl-glucosamine, D-maltose, potassium gluconate, capric acid, adipic acid, malic acid, trisodium citrate, and phenylacetic acid. Strain 23ND16S-022 displays the highest 16S rRNA gene sequence similarity with Sphingomonas aracearum WZY 27T (99.9%). Strain 23ND16S-022 (=NNIBR2023641BA2574=FBCC-B15826) was isolated from submerged sediment collected in Goseonggun, Gyeongsangnam-do, Korea (34°58ʹ53.3ʺN 128°13ʹ 18.4ʺE). The GenBank accession number of the 16S rRNA gene sequence is PP024215.

    3.5. Description of Sphingomonas glacialis 23ND19S-017

    Cells are Gram-stain-negative, non-flagellated, and rod-shaped. Colonies grown on R2A are circular, convex, and yellow after incubation for 7 days at 25°C. Positive for esculin hydrolysis, and β-galactosidase in API 20NE, but negative for nitrate reduction, indole production, glucose fermentation, arginine dihydrolase, urease, and gelatinase. Does not utilize D-glucose, L-arabinose, D-mannose, D-mannitol, N-acetyl-glucosamine, D-maltose, potassium gluconate, capric acid, adipic acid, malic acid, trisodium citrate, and phenylacetic acid. Strain 23ND19S-017 displays the highest 16S rRNA gene sequence similarity with Sphingomonas glacialis C16yT (99.2%). Strain 23ND19S-017 (=NNIBR 2023641BA2575=FBCC-B15825) was isolated from submerged sediment collected in Bonghwa-gun, Gyeongsangbuk- do, Korea (37°0ʹ58.19ʺN 128°43ʹ53.62ʺE). The GenBank accession number of the 16S rRNA gene sequence is PP024216.

    3.6. Description of Polymorphobacter multimanifer 23ND30S-6

    Cells are Gram-stain-negative, non-flagellated, and short rod-shaped. Colonies grown on NA are circular, convex, smooth, and brownish after incubation for 3 days at 25°C. Negative for nitrate reduction, indole production, glucose fermentation, arginine dihydrolase, urease, esculin hydrolysis, gelatinase, and β-galactosidase in API 20NE. Does not utilize D-glucose, L-arabinose, D-mannose, D-mannitol, N-acetyl-glucosamine, D-maltose, potassium gluconate, capric acid, adipic acid, malic acid, trisodium citrate, and phenylacetic acid. Strain 23ND30S-6 displays the highest 16S rRNA gene sequence similarity with Polymorphobacter multimanifer 262-7T (98.9%). Strain 23ND30S-6 (=NNIBR 2023641BA491=FBCC-B13563) was isolated from riverside sediment collected in Seongju-gun, Gyeongsangbuk- do, Korea (35°46ʹ26.46ʺN 128°25ʹ21.37ʺE). The GenBank accession number of the 16S rRNA gene sequence is PP024328.

    3.7. Description of Polymorphobacter fuscus 23ND04W-109

    Cells are Gram-stain-negative, non-flagellated, and short rod-shaped. Colonies grown on R2A are circular, convex, and orange-brown after incubation for 3 days at 25°C. Positive for esculin hydrolysis, gelatinase, and β-galactosidase in API 20NE, but negative for nitrate reduction, indole production, glucose fermentation, arginine dihydrolase, and urease. Does not utilize D-glucose, L-arabinose, D-mannose, D-mannitol, N-acetylglucosamine, D-maltose, potassium gluconate, capric acid, adipic acid, malic acid, trisodium citrate, and phenylacetic acid. Strain 23ND04W-109 displays the highest 16S rRNA gene sequence similarity with Polymorphobacter fuscus D40PT (99.2%). Strain 23ND04W-109 (=NNIBR2023641BA216=FBCC-B12939) was isolated from surface water collected in Andong-si, Gyeongsangbuk- do, Korea (35°37ʹ31.32ʺN 127°44ʹ20.35ʺE). The GenBank accession number of the 16S rRNA gene sequence is PP024223.

    3.8. Description of Croceibacterium mercurial 23ND33W-6

    Cells are Gram-stain-negative, non-flagellated, and short rod-shaped. Colonies grown on R2A are circular, convex, smooth, and yellow after incubation for 7 days at 25°C. Positive for esculin hydrolysis, gelatinase, and β-galactosidase in API 20NE, but negative for nitrate reduction, indole production, glucose fermentation, arginine dihydrolase, and urease. D-glucose, L-arabinose, and D-mannose are utilized. Does not utilize D-mannitol, N-acetyl-glucosamine, D-maltose, potassium gluconate, capric acid, adipic acid, malic acid, trisodium citrate, and phenylacetic acid. Strain 23ND33W-6 displays the highest 16S rRNA gene sequence similarity with Croceibacterium mercurial CoronadoT (99.8%). Strain 23ND33W-6 (=NNIBR2023641BA2585=FBCCB15850) was isolated from surface water collected in Geochang-gun, Gyeongsangnam-do, Korea (34°51ʹ 13.02ʺN 128°0ʹ35.54ʺE). The GenBank accession number of the 16S rRNA gene sequence is OR999585.

    3.9. Description of Devosia beringensis 23ND54W-032

    Cells are Gram-stain-negative, non-flagellated, and rod-shaped. Colonies grown on MA are circular, and light yellow after incubation for 7 days at 25°C. Positive for glucose fermentation, esculin hydrolysis, gelatinase, and β-galactosidase in API 20NE, but negative for nitrate reduction, indole production, arginine dihydrolase, and urease. D-mannitol and adipic acid are utilized. Does not utilize D-glucose, L-arabinose, D-mannose, N-acetyl-glucosamine, D-maltose, potassium gluconate, capric acid, malic acid, trisodium citrate, and phenylacetic acid. Strain 23ND54W-032 displays the highest 16S rRNA gene sequence similarity with Devosia beringensis S02T (99.4%). Strain 23ND54W-032 (=NNIBR 2023641BA2580=FBCC-B15820) was isolated from surface water collected in Samcheok-si, Gangwon-do, Korea (37°8ʹ59.4ʺN 129°18ʹ36.5ʺE). The GenBank accession number of the 16S rRNA gene sequence is PP024221.

    3.10. Description of Devosia crocina 23ND17S-33

    Cells are Gram-stain-negative, non-flagellated, and rod-shaped. Colonies grown on 0.1NA are circular, smooth, and white after incubation for 7 days at 25°C. Positive for nitrate reduction, urease, esculin hydrolysis, and β-galactosidase in API 20NE, but negative for indole production, glucose fermentation, arginine dihydrolase, and gelatinase. D-glucose, L-arabinose, and D-mannose, D-mannitol, N-acetyl-glucosamine, and D-maltose are utilized. Does not utilize potassium gluconate, capric acid, adipic acid, malic acid, trisodium citrate, and phenylacetic acid. Strain 23ND17S-33 displays the highest 16S rRNA gene sequence similarity with Devosia crocina IPL20T (98.9%). Strain 23ND 17S-33 (=NNIBR2023641BA2567=FBCC-B15833) was isolated from riverside sediment collected in Sacheon- si, Gyeongsangnam-do, Korea (35°0ʹ49.1ʺN 123° 8ʹ4.6ʺE). The GenBank accession number of the 16S rRNA gene sequence is OR999586.

    3.11. Description of Endobacterium cereale 23ND19W-039

    Cells are Gram-stain-negative, non-flagellated, and rod-shaped. Colonies grown on R2A are circular, smooth, and pale ivory after incubation for 7 days at 25°C. Positive for glucose fermentation, urease, esculin hydrolysis, and β-galactosidase in API 20NE, but negative nitrate reduction, indole production, arginine dihydrolase, and gelatinase. L-arabinose and malic acid are utilized. Does not utilize D-glucose, D-mannose, D-mannitol, N-acetyl-glucosamine, D-maltose, potassium gluconate, capric acid, adipic acid, trisodium citrate, and phenylacetic acid. Strain 23ND19W-039 displays the highest 16S rRNA gene sequence similarity with Endobacterium cereale RZME27T (99.2%). Strain 23ND19W-039 (=NNIBR2023641BA2576=FBCCB15824) was isolated from surface water collected in Bonghwa-gun, Gyeongsangbuk-do, Korea (37°0ʹ 58.19ʺN 128°43ʹ53.62ʺE). The GenBank accession number of the 16S rRNA gene sequence is PP024217.

    3.12. Description of Agaricicola taiwanensis JR11

    Cells are Gram-stain-negative, non-flagellated, and rod-shaped. Colonies grown on R2A are circular, convex, and yellow after incubation for 3 days at 25°C. Positive for esculin hydrolysis in API 20NE, but negative nitrate reduction, indole production, glucose fermentation, arginine dihydrolase, urease, gelatinase, and β-galactosidase. Malic acid is utilized. Does not utilize D-glucose, L-arabinose, D-mannose, D-mannitol, N-acetyl-glucosamine, D-maltose, potassium gluconate, capric acid, adipic acid, trisodium citrate, and phenylacetic acid. Strain JR11 displays the highest 16S rRNA gene sequence similarity with Agaricicola taiwanensis CC-SBABM117T (99.2%). Strain JR11 (=NNIBR 2017301BA4=FBCC-B3373) was isolated from hyporheic water collected in Yecheon-gun, Gyeongsangbukdo, Korea (36°34ʹ29.06ʺN 128°19ʹ16.68ʺE). The Gen- Bank accession number of the 16S rRNA gene sequence is MG818298.

    3.13. Description of Bradyrhizobium ingae JR13

    Cells are Gram-stain-negative, non-flagellated, and rod-shaped. Colonies grown on R2A are circular, convex, and white after incubation for 3 days at 25°C. Positive for nitrate reduction, indole production, urease, and esculin hydrolysis in API 20NE, but negative glucose fermentation, arginine dihydrolase, gelatinase, and β-galactosidase. Does not utilize D-glucose, L-arabinose, D-mannose, D-mannitol, N-acetyl-glucosamine, D-maltose, potassium gluconate, capric acid, adipic acid, malic acid, trisodium citrate, and phenylacetic acid. Strain JR13 displays the highest 16S rRNA gene sequence similarity with Bradyrhizobium ingae 51778T (99.1%). Strain JR11 (=NNIBR2017301BA5=FBCCB3374) was isolated from hyporheic water collected in Yecheon-gun, Gyeongsangbuk-do, Korea (36°34ʹ 29.06ʺN 128°19ʹ16.68ʺE). The GenBank accession number of the 16S rRNA gene sequence is MG818299.

    3.14. Description of Paracoccus everestensis 23ND53W-035

    Cells are Gram-stain-negative, non-flagellated, and cocci-shaped. Colonies grown on ISP4 are circular, convex, and orange after incubation for 7 days at 25°C. Positive for glucose fermentation, esculin hydrolysis, gelatinase, and β-galactosidase in API 20NE, but negative nitrate reduction, indole production, arginine dihydrolase, and urease. D-mannitol and adipic acid are utilized. Does not utilize D-glucose, L-arabinose, Dmannose, N-acetyl-glucosamine, D-maltose, potassium gluconate, capric acid, malic acid, trisodium citrate, and phenylacetic acid. Strain 23ND53W-035 displays the highest 16S rRNA gene sequence similarity with Paracoccus everestensis S8-55T (99.6%). Strain 23ND53W- 035 (=NNIBR2023641BA2579=FBCC-B15821) was isolated from surface water collected in Changwon-si, Gyeongsangnam-do, Korea (37°10ʹ52.7ʺN 129°19ʹ 40.7ʺE). The GenBank accession number of the 16S rRNA gene sequence is PP024220.

    3.15. Description of Pseudotabrizicola sediminis 23ND29W-22

    Cells are Gram-stain-negative, non-flagellated, and cocci-shaped. Colonies grown on ISP4 are circular, convex, and orange after incubation for 7 days at 25°C. Positive for nitrate reduction, esculin hydrolysis, and β-galactosidase in API 20NE, but negative indole production, glucose fermentation, arginine dihydrolase, urease, and gelatinase. Does not utilize D-glucose, L-arabinose, D-mannose, D-mannitol, N-acetyl-glucosamine, D-maltose, potassium gluconate, capric acid, adipic acid, malic acid, trisodium citrate, and phenylacetic acid. Strain 23ND29W-22 displays the highest 16S rRNA gene sequence similarity with Pseudotabrizicola sediminis DRYC-M-16T (99.1%). Strain 23ND 29W-22 (=NNIBR2023641BA1307=FBCC-B14353) was isolated from surface water collected in Changnyeong- gun, Gyeongsangnam-do, Korea (35°35ʹ35.41ʺ N 128°21ʹ38.02ʺE). The GenBank accession number of the 16S rRNA gene sequence is PP024330.

    3.16. Description of Undibacterium nitidum 23ND53W-014

    Cells are Gram-stain-negative, non-flagellated, and rod-shaped. Colonies grown on 0.1 MA are circular, convex, and pale white after incubation for 7 days at 25°C. Positive for nitrate reduction and esculin hydrolysis in API 20NE, but negative indole production, glucose fermentation, arginine dihydrolase, urease, gelatinase, and β-galactosidase. Does not utilize D-glucose, L-arabinose, D-mannose, D-mannitol, N-acetyl-glucosamine, D-maltose, potassium gluconate, capric acid, adipic acid, malic acid, trisodium citrate, and phenylacetic acid. Strain 23ND53W-014 displays the highest 16S rRNA gene sequence similarity with Undibacterium nitidum LX22WT (99.2%). Strain 23ND53W-014 (=NNIBR2023641BA2577=FBCC-B15823) was isolated from surface water collected in Changwon-si, Gyeongsangnam-do, Korea (37°10ʹ52.7ʺN 129°19ʹ40.7ʺ E). The GenBank accession number of the 16S rRNA gene sequence is PP024218.

    3.17. Description of Undibacterium umbellatum 23ND29W-88

    Cells are Gram-stain-negative, non-flagellated, and rod-shaped. Colonies grown on R2A are circular, convex, smooth, and white after incubation for 3 days at 25°C. Positive for nitrate reduction and esculin hydrolysis in API 20NE, but negative indole production, glucose fermentation, arginine dihydrolase, urease, gelatinase, and β-galactosidase. D-mannose, N-acetyl-glucosamine, D-maltose, adipic acid, and trisodium citrate are utilized. Does not utilize D-glucose, L-arabinose, D-mannitol, potassium gluconate, capric acid, malic acid, and phenylacetic acid. Strain 23ND29W-88 displays the highest 16S rRNA gene sequence similarity with Undibacterium umbellatum KW1T (99.6%). Strain 23ND29W-88 (=NNIBR2023641BA1326=FBCC-B14 372) was isolated from surface water collected in Changnyeong- gun, Gyeongsangnam-do, Korea (35°35ʹ35.41ʺ N 128°21ʹ38.02ʺE). The GenBank accession number of the 16S rRNA gene sequence is PP024329.

    3.18. Description of Azonexus fungiphilus 23ND53W-029

    Cells are Gram-stain-negative, non-flagellated, and rod-shaped. Colonies grown on R2A are circular, convex, and light ivory after incubation for 7 days at 25°C. Positive for esculin hydrolysis in API 20NE, but negative nitrate reduction, indole production, glucose fermentation, arginine dihydrolase, urease, gelatinase, and β-galactosidase. Potassium gluconate and malic acid are utilized. Does not utilize D-glucose, L-arabinose, D-mannose, D-mannitol, N-acetyl-glucosamine, Dmaltose, capric acid, adipic acid, trisodium citrate, and phenylacetic acid. Strain 23ND53W-029 displays the highest 16S rRNA gene sequence similarity with Azonexus fungiphilus DSM 23841T (99.8%). Strain 23ND 53W-029 (=NNIBR2023641BA2578=FBCC-B15822) was isolated from surface water collected in Changwonsi, Gyeongsangnam-do, Korea (37°10ʹ52.7ʺN 129°19ʹ 40.7ʺE). The GenBank accession number of the 16S rRNA gene sequence is PP024219.

    3.19. Description of Dechloromonas denitrificans 23ND17S-76

    Cells are Gram-stain-negative, non-flagellated, and rod-shaped. Colonies grown on 0.1 MA are small, circular, and white after incubation for 7 days at 25°C. Positive for nitrate reduction in API 20NE, but negative indole production, glucose fermentation, arginine dihydrolase, urease, esculin hydrolysis, gelatinase, and β- galactosidase. Does not utilize D-glucose, L-arabinose, D-mannose, D-mannitol, N-acetyl-glucosamine, Dmaltose, potassium gluconate, capric acid, adipic acid, malic acid, trisodium citrate, and phenylacetic acid. Strain 23ND17S-76 displays the highest 16S rRNA gene sequence similarity with Dechloromonas denitrificans ATCC BAA-841T (99.9%). Strain 23ND17S-76 (=NNIBR2023641BA2586=FBCC-B15851) was isolated from riverside sediment collected in Sacheon-si, Gyeongsangnam-do, Korea (35°0ʹ49.1ʺN 128°8ʹ4.6ʺE). The GenBank accession number of the 16S rRNA gene sequence is OR999587.

    3.20. Description of Acinetobacter tandoii 22ND44W-048

    Cells are Gram-stain-negative, non-flagellated, and rod-shaped. Colonies grown on 0.1 TSA are convex, circular, and pale white after incubation for 7 days at 25°C. Positive for esculin hydrolysis in API 20NE, but negative nitrate reduction, indole production, glucose fermentation, arginine dihydrolase, urease, gelatinase, and β-galactosidase. Capric acid, malic acid, trisodium citrate, and phenylacetic acid are utilized. Does not utilize utilize D-glucose, L-arabinose, D-mannose, D-mannitol, N-acetyl-glucosamine, D-maltose, potassium gluconate, and adipic acid. Strain 22ND44W-048 displays the highest 16S rRNA gene sequence similarity with Acinetobacter tandoii DSM 14970T (99.3%). Strain 22ND44W-048 (=NNIBR2023641BA2571=FBCCB15829) was isolated from surface water collected in Sacheon-si, Gyeongsangnam-do, Korea (35°03ʹ33.3ʺN 128°0ʹ49.8ʺE). The GenBank accession number of the 16S rRNA gene sequence is PP024212.

    3.21. Description of Budvicia aquatica 23ND30W-38

    Cells are Gram-stain-negative, non-flagellated, and rod-shaped. Colonies grown on MA are circular, convex, smooth, and beige after incubation for 3 days at 20°C. Positive for nitrate reduction and glucose fermentation in API 20NE, but negative indole production, arginine dihydrolase, urease, esculin hydrolysis, gelatinase, and β-galactosidase. D-glucose, L-arabinose, Dmannitol, N-acetyl-glucosamine, potassium gluconate, and malic acid are utilized. Does not utilize D-mannosel, D-maltose, capric acid, adipic acid, trisodium citrate, and phenylacetic acid. Strain 23ND30W-38 displays the highest 16S rRNA gene sequence similarity with Budvicia aquatica DSM 5075T (99.3%). Strain 23ND30W-38 (=NNIBR2023641BA470=FBCC-B13 542) was isolated from surface water collected in Seongju- gun, Gyeongsangbuk-do, Korea (35°46ʹ26.46ʺN 128°25ʹ21.37ʺE). The GenBank accession number of the 16S rRNA gene sequence is PP024327.

    3.22. Description of Streptomyces glauciniger 23ND22S-017

    Cells are Gram-stain-negative, non-flagellated, and filamentous-shaped. Colonies grown on 0.1 MA are circular, convex, and grey after incubation for 3 days at 20°C. Positive for esculin hydrolysis and gelatinase in API 20NE, but negative nitrate reduction, indole production, glucose fermentation, arginine dihydrolase, urease, and β-galactosidase. D-glucose, L-arabinose, D-mannosel, D-mannosel, D-maltose, potassium gluconate, adipic acid, and malic acid are utilized. Does not N-acetyl-glucosamine, capric acid, trisodium citrate, and phenylacetic acid. Strain 23ND22S-017 displays the highest 16S rRNA gene sequence similarity with Streptomyces glauciniger CGMCC 4.1858T (99.4%). Strain 23ND22S-017 (=NNIBR2023641BA329=FB CC-B13400) was isolated from riverside sediment collected in Uiseong-gun, Gyeongsangbuk-do, Korea (36° 31ʹ8.08ʺN 128°40ʹ28.01ʺE). The GenBank accession number of the 16S rRNA gene sequence is PP024225.

    3.23. Description of Streptomyces ossamyceticus 23ND29S-75

    Cells are Gram-stain-negative, non-flagellated, and rod-shaped. Colonies grown on R2A are irregular, rough, undulate, and beige after incubation for 3 days at 25°C. Positive for nitrate reduction, esculin hydrolysis, and β-galactosidase in API 20NE, but negative indole production, glucose fermentation, arginine dihydrolase, urease, and gelatinase. Does not utilize D-glucose, L-arabinose, D-mannose, D-mannitol, N-acetyl-glucosamine, D-maltose, potassium gluconate, capric acid, adipic acid, malic acid, trisodium citrate, and phenylacetic acid. Strain 23ND29S-75 displays the highest 16S rRNA gene sequence similarity with Streptomyces ossamyceticus NBRC 13983T (99.9%). Strain 23ND29S-75 (=NNIBR2023641BA2005=FBCC-B15035) was isolated from riverside sediment collected in Changnyeonggun, Gyeongsangnam-do, Korea (35°35ʹ35.41ʺN 128° 21ʹ38.02ʺE). The GenBank accession number of the 16S rRNA gene sequence is PP024331.

    3.24. Description of Nocardioides intraradicalis 23ND42S-12

    Cells are Gram-stain-negative, non-flagellated, and rod-shaped. Colonies grown on 0.1 MA are circular and pale yellow after incubation for 7 days at 25°C. Positive for nitrate reduction and β-galactosidase in API 20NE, but negative for indole production, glucose fermentation, arginine dihydrolase, urease, esculin hydrolysis, and gelatinase. Does not utilize D-glucose, L-arabinose, D-mannose, D-mannitol, N-acetyl-glucosamine, D-maltose, potassium gluconate, capric acid, adipic acid, malic acid, trisodium citrate, and phenylacetic acid. Strain 23ND42S-12 displays the highest 16S rRNA gene sequence similarity with Nocardioides intraradicalis YIM DR1091T (99.5%). Strain 23ND42S-12 (=NNIBR2023641BA2568=FBCC-B15830) was isolated from riverside sediment collected in Ulju-gun, Ulsan, Korea (35°3ʹ26ʺN 128°53ʹ1ʺE). The GenBank accession number of the 16S rRNA gene sequence is OR999588.

    3.25. Description of Mycobacterium komossense 23ND08W-19

    Cells are Gram-stain-negative, non-flagellated, and rod-shaped. Colonies grown on 0.1 MA are circular and pale yellow after incubation for 7 days at 25°C. Positive for nitrate reduction, esculin hydrolysis, and β-galactosidase in API 20NE, but negative for indole production, glucose fermentation, arginine dihydrolase, urease, and gelatinase. Does not utilize D-glucose, L-arabinose, D-mannose, D-mannitol, N-acetyl-glucosamine, D-maltose, potassium gluconate, capric acid, adipic acid, malic acid, trisodium citrate, and phenylacetic acid. Strain 23ND08W-19 displays the highest 16S rRNA gene sequence similarity with Mycobacterium komossense ATCC 33013T (99.0%). Strain 23ND 08W-19 (=NNIBR2023641BA2584=FBCC-B15849) was isolated from surface water collected in Sancheonggun, Gyeongsangnam-do, Korea (35°20ʹ28.42ʺN 127° 49ʹ47.61ʺE). The GenBank accession number of the 16S rRNA gene sequence is OR999584.

    3.26. Description of Cellulomonas carbonis 23ND29S-16

    Cells are Gram-stain-negative, non-flagellated, and rod-shaped. Colonies grown on MA are circular, convex, smooth, and yellowish after incubation for 3 days at 25°C. Positive for esculin hydrolysis and β-galactosidase in API 20NE, but negative for nitrate reduction, indole production, glucose fermentation, arginine dihydrolase, urease, and gelatinase. D-glucose and potassium gluconate are utilized. Does not utilize L-arabinose, D-mannose, D-mannitol, N-acetyl-glucosamine, D-maltose, capric acid, adipic acid, malic acid, trisodium citrate, and phenylacetic acid. Strain 23ND29S-16 displays the highest 16S rRNA gene sequence similarity with Cellulomonas carbonis T26T (99.2%). Strain 23ND29S-16 (=NNIBR2023641BA1366=FBCC-B14 377) was isolated from riverside sediment collected in Changnyeong-gun, Gyeongsangnam-do, Korea (35° 35ʹ35.41ʺN 128°21ʹ38.02ʺE). The GenBank accession number of the 16S rRNA gene sequence is PP024332.

    3.27. Description of Flavobacterium restrictum 23ND04S-005

    Cells are Gram-stain-negative, non-flagellated, and rod-shaped. Colonies grown on 0.1 R2A are convex and yellow after incubation for 3 days at 15°C. Positive for esculin hydrolysis and β-galactosidase in API 20NE, but negative for nitrate reduction, indole production, glucose fermentation, arginine dihydrolase, urease, and gelatinase. Does not utilize D-glucose, L-arabinose, D-mannose, D-mannitol, N-acetyl-glucosamine, D-maltose, potassium gluconate, capric acid, adipic acid, malic acid, trisodium citrate, and phenylacetic acid. Strain 23ND04S-005 displays the highest 16S rRNA gene sequence similarity with Flavobacterium restrictum LB1R34T (99.5%). Strain 23ND04S-005 (=NNIBR2023641BA184=FBCC-B12907) was isolated from riverside sediment collected in Andong-si, Gyeongsangbuk-do, Korea (35°37ʹ31.32ʺN 127°44ʹ 20.35ʺE). The GenBank accession number of the 16S rRNA gene sequence is PP024222.

    3.28. Description of Flavobacterium ammoniigenes 23ND49W-22

    Cells are Gram-stain-negative, non-flagellated, and rod-shaped. Colonies grown on 0.1 MA are small, circular, and yellow after incubation for 7 days at 25°C. Positive for nitrate reduction, esculin hydrolysis, and β-galactosidase in API 20NE, but negative for indole production, glucose fermentation, arginine dihydrolase, urease, and gelatinase. Does not utilize D-glucose, L-arabinose, D-mannose, D-mannitol, N-acetyl-glucosamine, D-maltose, potassium gluconate, capric acid, adipic acid, malic acid, trisodium citrate, and phenylacetic acid. Strain 23ND49W-22 displays the highest 16S rRNA gene sequence similarity with Flavobacterium ammoniigenes GENT5T (99.1%). Strain 23ND49W-22 (=NNIBR2023641BA2570=FBCCB15832) was isolated from surface water collected in Uljin-gun, Gyeongsangbuk-do, Korea (37°4ʹ24.57ʺN 129°23ʹ57.8ʺE). The GenBank accession number of the 16S rRNA gene sequence is OR999590.

    3.29. Description of Pedobacter cryoconitis JR29

    Cells are Gram-stain-negative, non-flagellated, and rod-shaped. Colonies grown on NA are circular, convex, mucoid, and cream after incubation for 3 days at 25°C. Positive for indole production, esculin hydrolysis, gelatinase, and β-galactosidase in API 20NE, but negative for nitrate reduction, glucose fermentation, arginine dihydrolase, and urease. D-glucose, L-arabinose, D-mannose, and D-maltose are utilized. Does not utilize D-mannitol, N-acetyl-glucosamine, potassium gluconate, capric acid, adipic acid, malic acid, trisodium citrate, and phenylacetic acid. Strain JR29 displays the highest 16S rRNA gene sequence similarity with Pedobacter cryoconitis PAMC 27485T (99.3%). Strain JR29 (=NNIBR2017301BA6=FBCC-B3383) was isolated from hyporheic water collected in Yecheon-gun, Gyeongsangbuk- do, Korea (36°34ʹ29.06ʺN 128°19ʹ16.68ʺE). The GenBank accession number of the 16S rRNA gene sequence is OR999590.

    ACKNOWLEDGEMENTS

    This study was supported by a grant from the Nakdonggang National Institute of Biological Resources (NNIBR), funded by the Ministry of Environment (MOE) of the Republic of Korea (NNIBR20241103).

    CRediT authorship contribution statement

    A Choi: Project administration, Conceptualization, Writing-Original draft, Funding acquisition, Writing- Reviewing and editing. JY Cho: Investigation, Data curation. SY Lee: Investigation, Data curation. JY Jung: Investigation, Data curation. K Baek: Investigation, Data curation. S Hwang: Investigation, Data curation. EJ Kim: Investigation, Data curation. J Goh: Supervision.

    Declaration of Competing Interest

    The authors declare no conflict of interest.

    Figure

    KJEB-42-2-143_F1.gif

    Neighbor-joining phylogenetic tree based on 16S rRNA gene sequences showing the relationship between the strains isolated in this study and their relatives in the class Alphaproteobacteria. Bootstrap values (>70%) are shown at nodes. Bar, 0.02 substitutions per nucleotide position.

    KJEB-42-2-143_F2.gif

    Neighbor-joining phylogenetic tree based on 16S rRNA gene sequences showing the relationship between the strains isolated in this study and their relatives in the classes Betaproteobacteria and Gammaproteobacteria. Bootstrap values (>70%) are shown at nodes. Bar, 0.02 substitutions per nucleotide position.

    KJEB-42-2-143_F3.gif

    Neighbor-joining phylogenetic tree based on 16S rRNA gene sequences showing the relationship between the strains isolated in this study and their relatives in the phylum Actinomycetota and Bacteroidota. Bootstrap values (>70%) are shown at nodes. Bar, 0.05 substitutions per nucleotide position.

    KJEB-42-2-143_F4.gif

    Transmission electron micrographs of cells of the strains isolated in this study. Strains: 1, 23ND15S-033; 2, 23ND23W-034; 3, 23ND49W-23; 4, 23ND16S-022; 5, 23ND19S-017; 6, 23ND30S -6; 7, 23ND04W-109; 8, 23ND33W-6; 9, 23ND54W-032; 10, 23ND17S-33; 11, 23ND19W-039; 12, JR11; 13, JR13; 14, 23ND53W-035; 15, 23ND29W-22; 16, 23ND53W-014; 17, 23ND29W-88; 18, 23ND53W-029; 19, 23ND17S-76; 20, 22ND44W-048; 21, 23ND30W-38; 22, 23ND22S-017; 23, 23ND29S-75; 24, 23ND42S-12; 25, 23ND08W-19; 26, 23ND29S-16; 27, 23ND04S-005; 28, 23ND49W-22; 29, JR29.

    Table

    Summary of unrecorded freshwater bacterial strains isolated from the Nakdonggang River and their taxonomic affiliations

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    Vol. 40 No. 4 (2022.12)

    Journal Abbreviation 'Korean J. Environ. Biol.'
    Frequency quarterly
    Doi Prefix 10.11626/KJEB.
    Year of Launching 1983
    Publisher Korean Society of Environmental Biology
    Indexed/Tracked/Covered By

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