Journal of Microbiology

Volume 57(5); May 2019

Review

MINIREVIEW] Dynamics of microbial communities and CO2 and CH4 fluxes in the tundra ecosystems of the changing Arctic: Min Jung Kwon , Ji Young Jung , Binu M. Tripathi , Mathias Göckede , Yoo Kyung Lee , Mincheol Kim; J. Microbiol. 2019;57(5):325-336. Published online January 16, 2019; DOI: https://doi.org/10.1007/s12275-019-8661-2

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Abstract: Arctic tundra ecosystems are rapidly changing due to the amplified effects of global warming within the northern high latitudes. Warming has the potential to increase the thawing of the permafrost and to change the landscape and its geochemical characteristics, as well as terrestrial biota. It is important to investigate microbial processes and community structures, since soil microorganisms play a significant role in decomposing soil organic carbon in the Arctic tundra. In addition, the feedback from tundra ecosystems to climate change, including the emission of greenhouse gases into the atmosphere, is substantially dependent on the compositional and functional changes in the soil microbiome. This article reviews the current state of knowledge of the soil microbiome and the two most abundant greenhouse gas (CO2 and CH4) emissions, and summarizes permafrost thaw-induced changes in the Arctic tundra. Furthermore, we discuss future directions in microbial ecological research coupled with its link to CO2 and CH4 emissions.

Journal Articles

Edaphovirga cremea gen. nov., sp. nov., isolated from the rhizospheric soil of Codonopsis clematidea: Jin-Yan Xue , Meng-Yue Zhang , Yu Zhang , Juan Cheng , Li-Cheng Liu , Ying-Ying Wu , Tian-Yuan Zhang , Yi-Xuan Zhang; J. Microbiol. 2019;57(5):337-342. Published online February 26, 2019; DOI: https://doi.org/10.1007/s12275-019-8408-0

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Abstract: A Gram-negative, facultatively anaerobic, non-motile, nonspore- forming, coccoid or rod-shaped and creamy-pigmented bacterium, designated SYP-B2100T, was isolated from the rhizospheric soil of Codonopsis clematidea in the Xinjiang Uygur Autonomous Region, China. The optimal growth occurred at 28°C, pH 5.0, in the absence of NaCl. The cells tested positive in catalase and methyl red tests but negative in oxidase, urease, gelatinase, milk coagulation, and peptonisation, H2S production, nitrate reduction, and Voges-Proskauer tests. The major isoprenoid quinone was ubiquinone-8 (Q-8). The major cellular fatty acids were C16:0 and summed feature 8. The polar lipids consisted of diphosphatidylglycerol, phosphatidylethanolamine, and phosphatidylglycerol. The 16S rRNA gene sequence of strain SYP-B2100T was the most similar to that of Rahnella inusitata DSM 30078T (96.9%) within the family Enterobacteriaceae. The genomic DNA G+C content of strain SYP-B2100T was 50.3 mol%. The combined data from the phylogenetic, morphological, physiological, biochemical, and chemotaxonomic analyses presented in this study support the conclusion that strain SYP-B2100T represents a novel species of a new genus, for which the name Edaphovirga cremea gen. nov., sp. nov. is proposed; the type strain is SYPB2100T (= CGMCC 1.5857T = DSM 105170T = KCTC 62024T).

Flavobacterium aquariorum sp. nov., isolated from freshwater of the North Han River: Yochan Joung , Hye-Jin Jang , Jaeho Song , Jang-Cheon Cho; J. Microbiol. 2019;57(5):343-349. Published online February 5, 2019; DOI: https://doi.org/10.1007/s12275-019-8436-9

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Abstract: A non-motile, yellow-pigmented bacterial strain, designated IMCC34762T, was isolated from a freshwater sample collected from Lake Cheongpyeong in Korea. Phylogenetic analysis based on 16S rRNA gene sequences showed that strain IMCC- 34762T formed a lineage within the genus Flavobacterium and was most closely related to F. pectinovorum DSM 6368T (98.3% sequence similarity), followed by F. piscis CCUG 60099T (98.3%), F. branchiicola 59B-3-09T (98.2%), and F. saccharophilum DSM 1811T (98.2%). The average nucleotide identity and the genome-to-genome distance between strain IMCC34762T and the closely related strains were 61–62% and 26–27%, respectively, indicating that IMCC34762T is a novel species of the genus Flavobacterium. The major fatty acids (> 5%) of strain IMCC34762T were summed feature 3 (C16:1 ω6c and/or C16:1 ω7c, 17.3%), iso-C15:0 (15.0%), iso-C15:0 G (9.0%), C15:0 ω6c (7.4%), iso-C15:0 (7.4%), and iso-C16:0 (5.3%). The major respiratory quinone and polyamine were MK-6 and sym-homospermidine, respectively. The major polar lipids were phosphatidylethanolamine, an unidentified aminophospholipid, and an unidentified lipid. The DNA G+C content of strain IMCC34762T was 34.4 mol%. Based on the taxonomic data presented in this study, strain IMCC34762T represents a novel species within the genus Flavobacterium, for which the name Flavobacterium aquariorum, sp. nov. is proposed. The type strain is IMCC34762T (= KACC 19725T = NBRC 113425T).

Acinetobacter chinensis, a novel Acinetobacter species, carrying blaNDM-1, recovered from hospital sewage: Yiyi Hu , Yu Feng , Jiayuan Qin , Xiaoxia Zhang , Zhiyong Zong; J. Microbiol. 2019;57(5):350-355. Published online February 26, 2019; DOI: https://doi.org/10.1007/s12275-019-8485-0

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Abstract: Two strains of the genus Acinetobacter, named WCHAc- 010005 and WCHAc010052, were isolated from hospital sewage at West China Hospital in Chengdu, China. The two strains were found to be resistant to carbapenems due to the presence of carbapenemase gene blaNDM-1. Based on the comparative analysis of the rpoB sequence, the two strains formed a strongly supported and internally coherent cluster (intracluster identity of 98.7%), which was clearly separated from all known Acinetobacter species (≤ 83.4%). The two strains also formed a tight and distinct cluster based on the genuswide comparison of whole-cell mass fingerprints generated by MALDI-TOF mass spectrometry. In addition, the combination of their ability to assimilate malonate but not benzoate, and the inability to grow at 37°C could distinguish the two strains from all known Acinetobacter species. The two strains were subjected to whole genome sequencing using both short-read Illumina HiSeq2500 platform and the longread MinION sequencer. The average nucleotide identity and in silico DNA-DNA hybridization value between the genomes of WCHAc010005 and WCHAc010052 was 96.69% and 74.3% respectively, whereas those between the two genomes and the known Acinetobacter species were < 80% and < 30%, respectively. Therefore, the two strains represent a novel species of the genus Acinetobacter, for which the name Acinetobacter chinensis sp. nov. is proposed, and the type strain is WCHAc- 010005T (= GDMCC 1.1232T = KCTC 62813T).

Mucibacter soli gen. nov., sp. nov., a new member of the family Chitinophagaceae producing mucin: Min-Kyeong Kim , Sewook Park , Tae-Su Kim , Yochan Joung , Ji-Hye Han , Seung Bum Kim; J. Microbiol. 2019;57(5):356-361. Published online February 22, 2019; DOI: https://doi.org/10.1007/s12275-019-8512-1

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Abstract: A Gram-stain-negative, mucus-forming, motile by gliding, non-spore-forming and short rod-shaped bacterial strain designated R1-15T was isolated from soil and its taxonomic position was evaluated using a polyphasic approach. Strain R1-15T grew at 15–37°C (optimum, 30°C), at pH 6–7 (optimum, pH 6) and in the presence of 0–1% (w/v) NaCl (optimum, 0%) on 0.1X TSA. On the basis of 16S rRNA gene sequence similarity, the novel strain was assigned to the family Chitinophagaceae of the phylum Bacteroidetes, and its closest related taxa were species of the genera Taibaiella (88.76– 90.02% sequence similarity), Lacibacter (89.24–90.00%), Chitinophaga (88.61–89.76%), and Terrimonas (89.04%). Flexirubin- type pigments were produced. The only isoprenoid quinone was MK-7, and the major polar lipid was phosphatidylethanolamine. Based on whole genome comparisons between the strain R1-15T and the type strains of relatives, the orthologous average nucleotide identity values were 66.9– 67.0%. The DNA G+C content of strain R1-15T was 43.8 mol%. The combination of phylogenetic, chemotaxonomic and phenotypic data clearly supported separation of strain R1-15T from related taxa, and thus the name Mucibacter soli gen. nov., sp. nov. is proposed. The type strain is R1-15T (= KCTC 62274T = JCM 31190T).

Microbial transformation of Se oxyanions in cultures of Delftia lacustris grown under aerobic conditions: Shrutika L. Wadgaonkar , Yarlagadda V. Nancharaiah , Claus Jacob , Giovanni Esposito , Piet N. L. Lens; J. Microbiol. 2019;57(5):362-371. Published online March 21, 2019; DOI: https://doi.org/10.1007/s12275-019-8427-x

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Abstract: Delftia lacustris is reported for the first time as a selenate and selenite reducing bacterium, capable of tolerating and growing in the presence of ≥ 100 mM selenate and 25 mM selenite. The selenate reduction profiles of D. lacustris were investigated by varying selenate concentration, inoculum size, concentration and source of organic electron donor in minimal salt medium. Interestingly, the bacterium was able to reduce both selenate and selenite under aerobic conditions. Although considerable removal of selenate was observed at all concentrations investigated, D. lacustris was able to completely reduce 0.1 mM selenate within 96 h using lactate as the carbon source. Around 62.2% unaccounted selenium (unidentified organo-selenium compounds), 10.9% elemental selenium and 26.9% selenite were determined in the medium after complete reduction of selenate. Studies of the enzymatic activity of the cell fractions show that the selenite/selenate reducing enzymes were intracellular and independent of NADPH availability. D. lacustris shows an unique metabolism of selenium oxyanions to form elemental selenium and possibly also selenium ester compounds, thus a potential candidate for the remediation of selenium-contaminated wastewaters in aerobic environments. This novel finding will advance the field of bioremediation of selenium-contaminated sites and selenium bio-recovery and the production of potentially beneficial organic and inorganic reactive selenium species.

Identification and characterization of a marine-derived chitinolytic fungus, Acremonium sp. YS2-2: Dawoon Chung , Kyunghwa Baek , Seung Seob Bae , Jaejoon Jung; J. Microbiol. 2019;57(5):372-380. Published online February 26, 2019; DOI: https://doi.org/10.1007/s12275-019-8469-0

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Abstract: Chitin is the most abundant biopolymer in marine environments. To facilitate its utilization, our laboratory screened marine-derived fungal strains for chitinolytic activity. One chitinolytic strain isolated from seawater, designated YS2-2, was identified as Acremonium species based on morphological and phylogenetic analyses. Acremonium species are cosmopolitan fungi commonly isolated from both terrestrial and marine environments, but their chitinolytic activity is largely unknown. The extracellular crude enzyme of YS2-2 exhibited optimum chitinolytic activity at pH 6.0–7.6, 23–45°C, and 1.5% (w/v) NaCl. Degenerate PCR revealed the partial cDNA sequence of a putative chitinase gene, chiA, in YS2-2. The expression of chiA was dramatically induced in response to 1% (w/v) colloidal chitin compared to levels under starvation, chitin powder, and glucose conditions. Moreover, the chiA transcript levels were positively correlated with chitinolytic activities under various colloidal chitin concentrations, suggesting that ChiA mediates chitinolytic activity in this strain. Our results provide a basis for additional studies of marinederived chitinolytic fungi aimed at improving industrial applications.

Intestinibaculum porci gen. nov., sp. nov., a new member of the family Erysipelotrichaceae isolated from the small intestine of a swine: Ji-Sun Kim , Hanna Choe , Yu-Ri Lee , Kyung Mo Kim , Doo-Sang Park; J. Microbiol. 2019;57(5):381-387. Published online February 22, 2019; DOI: https://doi.org/10.1007/s12275-019-8631-8

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Abstract: A strictly anaerobic, Gram-stain-positive, catalase-negative, non-motile, rod-shaped bacterium, designated SG0102T, was isolated from the small intestine of a swine. Optimal growth occurred at 37°C and pH 7.0. Furthermore, growth was observed in the presence of up to 3% (w/v) NaCl but not at salinity levels higher than 4%. The comparative analysis of 16S rRNA gene sequences showed that strain SG0102T was most closely related to Kandleria vitulina DSM 20405T (93.3%), followed by Catenibacterium mitsuokai KCTC 5053T (91.1%), Sharpea azabuensis KCTC 15217T (91.0%), and Eggerthia catenaformis DSM 5348T (89.6%). The average nucleotide identity values between strain SG0102T and related species, K. vitulina DSM 20405T, C. mitsuokai KCTC 5053T, S. azabuensis KCTC 15217T, and E. catenaformis DSM 5348T, were 71.0, 69.3, 70.0, and 69.2%, respectively. The phylogenetic analysis based on 16S rRNA gene sequence revealed that strain SG0102T belonged to the family Erysipelotrichaceae in the class Erysipelotrichia. The DNA G+C content of the strain SG0102T was 39.5 mol%. The major cellular fatty acids (> 10%) of strain SG0102T were C16:0, C16:0 dimethyl acetal, and C18:2 ω9/12c. The cell wall peptidoglycan of strain SG0102T contained the meso-diaminopimelic acid. The strain SG0102T produced lactic acid as a major end product of fermentation. These distinct phenotypic and phylogenetic properties suggest that strain SG0102T represents a novel species in a novel genus of the family Erysipelotrichaceae, for which the name Intestinibaculum porci gen. nov. sp. nov. is proposed. The type strain is SG0102T (= KCTC 15725T = NBRC 113396T).

Growth and differentiation properties of pikromycin-producing Streptomyces venezuelae ATCC15439: Ji-Eun Kim , Joon-Sun Choi , Jung-Hye Roe; J. Microbiol. 2019;57(5):388-395. Published online February 5, 2019; DOI: https://doi.org/10.1007/s12275-019-8539-3

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Abstract: Streptomycetes naturally produce a variety of secondary metabolites, in the process of physiological differentiation. Streptomyces venezuelae differentiates into spores in liquid media, serving as a good model system for differentiation and a host for exogenous gene expression. Here, we report the growth and differentiation properties of S. venezuelae ATCC- 15439 in liquid medium, which produces pikromycin, along with genome-wide gene expression profile. Comparison of growth properties on two media (SPA, MYM) revealed that the stationary phase cell viability rapidly decreased in SPA. Submerged spores showed partial resistance to lysozyme and heat, similar to what has been observed for better-characterized S. venezuelae ATCC10712, a chloramphenicol producer. TEM revealed that the differentiated cells in the submerged culture showed larger cell size, thinner cell wall than the aerial spores. We analyzed transcriptome profiles of cells grown in liquid MYM at various growth phases. During transition and/or stationary phases, many differentiationrelated genes were well expressed as judged by RNA level, except some genes forming hydrophobic coats in aerial mycelium. Since submerged spores showed thin cell wall and partial resistance to stresses, we examined cellular expression of MreB protein, an actin-like protein known to be required for spore wall synthesis in Streptomycetes. In contrast to aerial spores where MreB was localized in septa and spore cell wall, submerged spores showed no detectable signal. Therefore, even though the mreB transcripts are abundant in liquid medium, its protein level and/or its interaction with spore wall synthetic complex appear impaired, causing thinner- walled and less sturdy spores in liquid culture.

Biocontrol activity of volatile organic compounds from Streptomyces alboflavus TD-1 against Aspergillus flavus growth and aflatoxin production: Mingguan Yang , Laifeng Lu , Jing Pang , Yiling Hu , Qingbin Guo , Zhenjing Li , Shufen Wu , Huanhuan Liu , Changlu Wang; J. Microbiol. 2019;57(5):396-404. Published online May 6, 2019; DOI: https://doi.org/10.1007/s12275-019-8517-9

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Abstract: Aspergillus flavus is a saprophytic fungus that contaminates crops with carcinogenic aflatoxin. In the present work, the antifungal effects of volatile organic compounds (VOCs) from Streptomyces alboflavus TD-1 against A. flavus were investigated. VOCs from 8-day-old wheat bran culture of S. alboflavus TD-1 displayed strong inhibitory effects against mycelial growth, sporulation, and conidial germination of A. flavus. Severely misshapen conidia and hyphae of A. flavus were observed by scanning electron microscopy after exposure to VOCs for 6 and 12 h, respectively. Rhodamine 123 staining of mitochondria indicated that mitochondria may be a legitimate antifungal target of the VOCs from S. alboflavus TD-1. Furthermore, the VOCs effectively inhibited aflatoxin B1 production by downregulating genes involved in aflatoxin biosynthesis. Dimethyl trisulfide and benzenamine may play important roles in the suppression of A. flavus growth and production of aflatoxin. The results indicate that VOCs from S. alboflavus TD-1 have tremendous potential to be developed as a useful bio-pesticide for controlling A. flavus.

Expansion of antibacterial spectrum of xanthorrhizol against Gram-negatives in combination with PMBN and food-grade antimicrobials: Man Su Kim , Ha-Rim Kim , Haebom Kim , Soo-Keun Choi , Chang-Hwan Kim , Jae-Kwan Hwang , Seung-Hwan Park; J. Microbiol. 2019;57(5):405-412. Published online February 22, 2019; DOI: https://doi.org/10.1007/s12275-019-8511-2

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Abstract: Xanthorrhizol (XTZ), isolated from Curcuma xanthorrhiza, has potent antifungal and antibacterial activity. It shows very strong activity against Gram-positive bacteria, such as Streptococcus mutans and Staphylococcus aureus, but is generally not active against Gram-negative bacteria. In this study, we explored the possibility of using a combination strategy for expanding the antimicrobial spectrum of XTZ against Gram-negative bacteria. To take advantage of XTZ being a food-grade material, 10 food-grade or generally recognized as safe (GRAS) antimicrobial compounds with low toxicities were selected for combination therapy. In addition, polymyxin B nonapeptide (PMBN), which is less toxic than polymyxin B, was also selected as an outer membrane permeabilizer. The antibacterial activity of various double or triple combinations with or without XTZ were assayed in vitro against four Gram-negative bacterial species (Escherichia coli, Salmonella enterica serovar Typhi, Salmonella enterica serovar Typhimurium, and Vibrio cholerae), with synergistic combinations exhibiting clear activity subjected to further screening. The combinations with the greatest synergism were XTZ + PMBN + nisin, XTZ + PMBN + carvacrol, and XTZ + PMBN + thymol. These combinations also showed potent antimicrobial activity against Shigella spp., Yersinia enterocolitica, and Acinetobacter baumannii. In time-kill assays, the three combinations achieved complete killing of E. coli within 2 h, and S. Typhi and V. cholera within 15 min. This is the first report on expanding the activity spectrum of XTZ against Gram-negative bacteria through combination with PMBN and food-grade or GRAS substances, with the resulting findings being particularly useful for increasing the industrial and medical applications of XTZ.

Genome analysis of Rubritalea profundi SAORIC-165T, the first deep-sea verrucomicrobial isolate, from the northwestern Pacific Ocean: Jaeho Song , Ilnam Kang , Yochan Joung , Susumu Yoshizawa , Ryo Kaneko , Kenshiro Oshima , Masahira Hattori , Koji Hamasaki , Soochan Kim , Kangseok Lee , Jang-Cheon Cho; J. Microbiol. 2019;57(5):413-422. Published online February 26, 2019; DOI: https://doi.org/10.1007/s12275-019-8712-8

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Abstract: Although culture-independent studies have shown the presence of Verrucomicrobia in the deep sea, verrucomicrobial strains from deep-sea environments have been rarely cultured and characterized. Recently, Rubritalea profundi SAORIC- 165T, a psychrophilic bacterium of the phylum Verrucomicrobia, was isolated from a depth of 2,000 m in the northwestern Pacific Ocean. In this study, the genome sequence of R. profundi SAORIC-165T, the first deep-sea verrucomicrobial isolate, is reported with description of the genome properties and comparison to surface-borne Rubritalea genomes. The draft genome consisted of four contigs with an entire size of 4,167,407 bp and G+C content of 47.5%. The SAORIC-165T genome was predicted to have 3,844 proteincoding genes and 45 non-coding RNA genes. The genome contained a repertoire of metabolic pathways, including the Embden-Meyerhof-Parnas pathway, pentose phosphate pathway, tricarboxylic acid cycle, assimilatory sulfate reduction, and biosynthesis of nicotinate/nicotinamide, pantothenate/ coenzyme A, folate, and lycopene. The comparative genomic analyses with two surface-derived Rubritalea genomes showed that the SAORIC-165T genome was enriched in genes involved in transposition of mobile elements, signal transduction, and carbohydrate metabolism, some of which might be related to bacterial enhancement of ecological fitness in the deep-sea environment. Amplicon sequencing of 16S rRNA genes from the water column revealed that R. profundi-related phylotypes were relatively abundant at 2,000 m and preferred a particle-associated life style in the deep sea. These findings suggest that R. profundi represents a genetically unique and ecologically relevant verrucomicrobial group well adapted to the deep-sea environment.

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