Enantioselective Utilization of D-Amino Acids by Deep-Sea Microorganisms

Kubota, Takaaki; Kobayashi, Tohru; Nunoura, Takuro; Maruyama, Fumito; Deguchi, Shigeru

doi:10.3389/fmicb.2016.00511

Cited by 31 publications

(34 citation statements)

References 66 publications

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“…This has been interpreted as evidence that mesopelagic prokaryotic plankton are using bacterial cell wall-derived organic matter because the bacterial peptidoglycan layer is the only major biotic source of significant D-amino acids in the ocean (31). However, information about D-amino acid utilization by marine microbes remains limited (32).…”

Section: Discussionmentioning

confidence: 99%

Pangenomics Analysis Reveals Diversification of Enzyme Families and Niche Specialization in Globally Abundant SAR202 Bacteria

Saw

Nunoura

Hirai

et al. 2020

mBio

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It has been hypothesized that the abundant heterotrophic ocean bacterioplankton in the SAR202 clade of the phylum Chloroflexi evolved specialized metabolisms for the oxidation of organic compounds that are resistant to microbial degradation via common metabolic pathways. Expansions of paralogous enzymes were reported and implicated in hypothetical metabolism involving monooxygenase and dioxygenase enzymes. In the proposed metabolic schemes, the paralogs serve the purpose of diversifying the range of organic molecules that cells can utilize. To further explore SAR202 evolution and metabolism, we reconstructed single amplified genomes and metagenome-assembled genomes from locations around the world that included the deepest ocean trenches. In an analysis of 122 SAR202 genomes that included seven subclades spanning SAR202 diversity, we observed additional evidence of paralog expansions that correlated with evolutionary history, as well as further evidence of metabolic specialization. Consistent with previous reports, families of flavin-dependent monooxygenases were observed mainly in the group III SAR202 genomes, and expansions of dioxygenase enzymes were prevalent in those of group VII. We found that group I SAR202 genomes encode expansions of racemases in the enolase superfamily, which we propose evolved for the degradation of compounds that resist biological oxidation because of chiral complexity. Supporting the conclusion that the paralog expansions indicate metabolic specialization, fragment recruitment and fluorescent in situ hybridization (FISH) with phylogenetic probes showed that SAR202 subclades are indigenous to different ocean depths and geographical regions. Surprisingly, some of the subclades were abundant in surface waters and contained rhodopsin genes, altering our understanding of the ecological role of SAR202 species in stratified water columns. IMPORTANCE The oceans contain an estimated 662 Pg C in the form of dissolved organic matter (DOM). Information about microbial interactions with this vast resource is limited, despite broad recognition that DOM turnover has a major impact on the global carbon cycle. To explain patterns in the genomes of marine bacteria, we propose hypothetical metabolic pathways for the oxidation of organic molecules that are resistant to oxidation via common pathways. The hypothetical schemes we propose suggest new metabolic pathways and classes of compounds that could be important for understanding the distribution of organic carbon throughout the biosphere. These genome-based schemes will remain hypothetical until evidence from experimental cell biology can be gathered to test them. Our findings also fundamentally change our understanding of the ecology of SAR202 bacteria, showing that metabolically diverse variants of these cells occupy niches spanning all depths and are not relegated to the dark ocean.

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Section: Discussionmentioning

confidence: 99%

Pangenomics Analysis Reveals Diversification of Enzyme Families and Niche Specialization in Globally Abundant SAR202 Bacteria

Saw

Nunoura

Hirai

et al. 2020

mBio

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“…Although there is a considerable amount of DAAs derived from bacterial peptidoglycan and released by microorganisms in the ocean, only a few DAA-utilizing bacteria have been reported. Kubota et al (2016) reported 28 marine DAAutilizing bacterial strains from the classes Alphaproteobacteria, Gammaproteobacteria and Bacilli. The results presented herein indicate that there are likely a larger number of DAA-utilizing bacteria in the ocean.…”

Section: Discussionmentioning

confidence: 99%

“…There is currently only one report on an investigation of the diversity of DAA-utilizing microbes. Kubota et al (2016) isolated 28 DAA-utilizing bacterial strains from deep-sea sediments, which were then phylogenetically assigned to Alphaproteobacteria, Gammaproteobacteria, and Bacilli. In addition to these bacterial strains, more DAA-utilizing microbes can be expected to be identified due to the ubiquity of DAAs in the ocean.…”

Section: Introductionmentioning

confidence: 99%

Diversity of D-Amino Acid Utilizing Bacteria From Kongsfjorden, Arctic and the Metabolic Pathways for Seven D-Amino Acids

Yang

Zheng

et al. 2020

Front. Microbiol.

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D-amino acids (DAAs) are an important component of the refractory dissolved organic matter pool in the ocean. Microbes play a vital role in promoting the recycling of DAAs in the ocean. However, the diversity of marine DAA-utilizing bacteria and how they metabolize DAAs are seldom studied. Here, by enrichment culture with DAAs as the sole nitrogen source, bacteria of 12 families from three phyla were recovered from surface seawater and sediment from Kongsfjorden, Arctic, and seven DAA-utilizing bacterial strains were isolated. These strains have different DAA-utilizing abilities. Of the seven DAAs used, Halomonas titanicae SM1922 and Pseudoalteromonas neustonica SM1927 were able to utilize seven and five of them, respectively, while the other strains were able to utilize only one or two. Based on genomic, transcriptional and biochemical analyses, the key genes involved in DAA metabolism in each strain were identified and the metabolic pathways for the seven DAAs in these marine bacteria were identified. Conversion of DAAs into α-keto acids is generally the main pathway in marine DAA-utilizing bacteria, which is performed by several key enzymes, including DAA oxidoreductases/dehydrogenases, D-serine ammonia-lyases, D-serine ammonialyase DSD1s and DAA transaminases. In addition, conversion of DAAs into LAAs is another pathway, which is performed by amino acid racemases. Among the identified key enzymes, D-serine ammonia-lyase DSD1 and Asp racemase are first found to be employed by bacteria for DAA utilization. These results shed light on marine DAA-utilizing bacteria and the involved DAA metabolism pathways, offering a better understanding of the DAA recycling in the ocean.

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“…This has been interpreted as evidence that mesopelagic prokaryotic plankton are using bacterial cell wall–derived organic matter because the bacterial peptidoglycan layer is the only major biotic source of significant of D–amino acids in the ocean (37). However, information about D-amino utilization by marine microbes remains limited (38).…”

Section: Discussionmentioning

confidence: 99%

Pangenomics reveal diversification of enzyme families and niche specialization in globally abundant SAR202 bacteria

Saw

Nunoura

Hirai

et al. 2019

Preprint

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Enantioselective Utilization of D-Amino Acids by Deep-Sea Microorganisms

Cited by 31 publications

References 66 publications

Pangenomics Analysis Reveals Diversification of Enzyme Families and Niche Specialization in Globally Abundant SAR202 Bacteria

Pangenomics Analysis Reveals Diversification of Enzyme Families and Niche Specialization in Globally Abundant SAR202 Bacteria

Diversity of D-Amino Acid Utilizing Bacteria From Kongsfjorden, Arctic and the Metabolic Pathways for Seven D-Amino Acids

Pangenomics reveal diversification of enzyme families and niche specialization in globally abundant SAR202 bacteria

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