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. 2022 May 23:13:868728.
doi: 10.3389/fmicb.2022.868728. eCollection 2022.

Characterization of a Deep-Sea Actinobacterium Strain Uncovers Its Prominent Capability of Utilizing Taurine and Polyvinyl Alcohol

Yingqi Tan  1   2   3   4 , Yeqi Shan  1   2   3   4 , Rikuan Zheng  1   2   3   4 , Rui Liu  1   2   4 , Chaomin Sun  1   2   3   4
Affiliations

Characterization of a Deep-Sea Actinobacterium Strain Uncovers Its Prominent Capability of Utilizing Taurine and Polyvinyl Alcohol

Yingqi Tan et al. Front Microbiol. .

Abstract

Actinobacteria represent a large group of important prokaryotes with great application potentials and widely distribute in diverse natural environments including the ocean. However, compared to their terrestrial cultured members, there are much less available marine Actinobacteria, especially deep-sea counterparts. Here, we cultured a bacterial strain of deep-sea actinobacterium, Marmoricola sp. TYQ2, by using a basal medium supplemented with taurine. Consistently, the growth of strain TYQ2 was significantly promoted by the supplement of taurine. Transcriptomic analysis showed that the expressions of genes encoding proteins associated with taurine metabolization and utilization as well as energy generation were evidently up-regulated when taurine was added. Moreover, strain TYQ2 was demonstrated to degrade polyvinyl alcohol (PVA) with the involvement of the redox cycle of extracellular quinol and quinone and the reduction of iron to ferrous, and strain TYQ2 could utilize the degradation products for energy production, thereby supporting bacterial growth. Overall, our experimental results demonstrate the prominent degradation capabilities of Marmoricola sp. TYQ2 toward the organics taurine and PVA.

Keywords: actinomyces; cultivation; deep sea; polyvinyl alcohol; taurine.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

FIGURE 1
FIGURE 1
Cultivation, morphology, and phylogeny of Marmoricola sp. TYQ2 isolated from the deep-sea cold seep. (A) Diagram of enrichment and cultivation of strain TYQ2 by using a taurine supplemented medium. (B) Observation of the cell morphology of strain TYQ2 through the transmission electron microscopy. Bar is 1 μm. (C) Maximum likelihood 16S rRNA gene phylogenetic tree showing the position of strain TYQ2 as well as the family Nocardioidaceae within the Actinobacteria phylum. The accession number of each 16S rRNA gene is shown in the parentheses after corresponding strain name. The numbers by the side of branch node indicated statistical support for bootstrap values, respectively. Scale bar, 0.1 substitutions per nucleotide position.
FIGURE 2
FIGURE 2
Strain TYQ2 effectively utilizes taurine. (A) Growth assays of strain TYQ2 in the 1/10 2216E medium supplemented either without or with 40 mM taurine. (B) A heat map based on transcriptomics analysis showing the up-regulated genes associated with taurine and sulfonate transport. (C) A heat map based on transcriptomics analysis showing the up-regulated genes associated with the metabolism of taurine. (D) A heat map based on transcriptomics showing the up-regulated genes involved in metabolites export.
FIGURE 3
FIGURE 3
Transcriptomic analysis of essential metabolic pathways for energy production in strain TYQ2 that cultured in the medium supplemented with taurine. (A) A heat map based on transcriptomics showing the up-regulated genes involved in acetyl-CoA synthesis and metabolism and the tricarboxylic acid cycle. (B) The diagram of the tricarboxylic acid cycle of strain TYQ2. The gene numbers are the same to those shown in panel (A). (C) A heat map based on transcriptomics showing all the up-regulated genes involved in sugar transport and metabolism. (D) A heat map based on transcriptomics showing all up-regulated genes related to lipid metabolism. (E) Transcriptomics-based heat map showing all up-regulated genes related to amino acid and nucleotide metabolism. (F) A heat map based on transcriptomics showing all up-regulated genes encoding iron-sulfur proteins. (G) A heat map based on transcriptomics showing the up-regulation of all genes related to NAD(P)/FAD/NADH oxidoreductase and ATPase.
FIGURE 4
FIGURE 4
Strain TYQ2 effectively utilizes PVA. (A) Growth assays of strain TYQ2 in the 1/10 2216E medium supplemented either without or with 10 g/L PVA. (B) A heat map based on transcriptomics analysis showing the up-regulation of genes encoding the quinone reductase and quinol monooxygenase. (C) A heat map based on transcriptomics analysis showing the up-regulated genes related to iron/ferrous iron transmembrane transporters and relevant FAD/ATP-binding proteins. (D) The proposed Fenton reaction driven by the redox process of quinone and quinol. Q, quinone; H2Q, quinol; HQ, semiquinone; OOH, perhydroxyl radical.
FIGURE 5
FIGURE 5
Transcriptomic analysis of essential metabolic pathways for energy production in strain TYQ2 that cultured in the medium supplemented with PVA. (A) A heat map based on transcriptomics analysis showing the up-regulated genes related to lipid metabolism. (B) A heat map based on transcriptomics showing all the up-regulated genes associated with sugar/amino acid/nucleotide metabolism. (C) A heat map based on transcriptomics analysis showing all up-regulated genes related to tricarboxylic acid cycle. (D) A heat map based on transcriptomics analysis showing all up-regulated genes encoding proteins associated with ATP generation.
FIGURE 6
FIGURE 6
Diagram of a proposed model describing degradation and utilization of taurine and PVA by Marmoricola sp. TYQ2. In this model, the metabolization of taurine and PVA as well as the contribution to energy production was highlighted. ThDP, thiamine diphosphate; Pi, phosphate group.
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