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Sulfitobacter alexandrii sp. nov., a new microalgae growth-promoting bacterium with exopolysaccharides bioflocculanting potential isolated from marine phycosphere

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Abstract

Marine phycosphere harbors unique cross-kingdom associations with enormous ecological significance in aquatic ecosystems as well as relevance for algal biotechnology industry. During our investigating the microbial composition and bioactivity of marine phycosphere microbiota (PM), a novel lightly yellowish and versatile bacterium designated strain AM1-D1T was isolated from cultivable PM of marine dinoflagellate Alexandrium minutum amtk4 that produces high levels of paralytic shellfish poisoning toxins (PSTs). Strain AM1-D1T demonstrates notable bioflocculanting bioactivity with bacterial exopolysaccharides (EPS), and microalgae growth-promoting (MGP) potential toward its algal host. Phylogenetic analysis based on 16S rRNA gene sequences revealed that strain AM1-D1T was affiliated to the members of genus Sulfitobacter within the family Rhodobacteraceae, showing the highest sequence similarity of 97.9% with Sulfitobacter noctilucae NB-68T, and below 97.8% with other type strains. The complete genome of strain AM1-D1T consisted of a circular 3.84-Mb chromosome and five circular plasmids (185, 95, 15, 205 and 348 Kb, respectively) with the G+C content of 64.6%. Low values obtained by phylogenomic calculations on the average nucleotide identity (ANI, 77.2%), average amino acid identity (AAI, 74.7%) and digital DNA-DNA hybridization (dDDH, 18.6%) unequivocally separated strain AM1-D1T from its closest relative. The main polar lipids were identified as phosphatidylglycerol, phosphatidylethanolamine, phosphatidylcholine, diphosphatidylglycerol, one unidentified phospholipid and one unidentified lipid. The predominant fatty acids (> 10%) were C18:1 ω7c, C19:0 cyclo ω8c and C16:0. The respiratory quinone was Q-10. The genome of strain AM1-D1T was predicted to encode series of gene clusters responsible for sulfur oxidation (sox) and utilization of dissolved organic sulfur exometabolites from marine dinoflagellates, taurine (tau) and dimethylsulfoniopropionate (DMSP) (dmd), as well as supplementary vitamin B12 (cob), photosynthesis carotenoids (crt) which are pivotal components during algae-bacteria interactions. Based on the evidences by the polyphasic characterizations, strain AM1-D1T represents a novel species of the genus Sulfitobacter, for which the name Sulfitobacter alexandrii sp. nov. is proposed. The type strain is AM1-D1T (= CCTCC 2017277T = KCTC 62491T).

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Availability of data and materials

Strain AM1-D1T has been deposited in two independent international culture centers (CCTCC in China, and KCTC in South Korea) with the deposition no. CCTCC AB 201696 and KCTC 52626, respectively.

Abbreviations

AAI:

Average amino acid identity

ABI:

Algae-bacteria interactions

ANI:

Average nucleotide identity

MGPB:

Microalgae growth-promoting bacteria

dDDH:

Digital DNA–DNA hybridization

DPG:

Diphosphatidylglycerol

DMSP:

Dimethylsulfoniopropionate

EPS:

Exopolysaccharides

HAB:

Harmful algal blooms

MA:

Marine agar

MB:

Marine broth

ML:

Maximum likelihood

MP:

Maximum parsimony

NJ:

Neighbour joining

PC:

Phosphatidylcholine

PE:

Phosphatidylethanolamine

PG:

Phosphatidylglycerol

PHB:

Polyhydroxybutyrate

PL:

Phospholipids

PM:

Phycosphere microbiota

PMP:

Phycosphere microbiome project

UBCG:

Up-to-date bacterial core gene

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Acknowledgements

We are grateful to Prof. Hong-non Chou at National Taiwan University for kindly providing the marine dinoflagellate Alexandrium minutum amtk4. This work was supported by the National Natural Science Foundation of China (41876114), Key Research and Development Program of Guangdong (2020B0202080004), Special Fund of Yinling of Guangdong (2020A1313030131), and the Natural Science Foundation of Zhejiang (LY18D060007).

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Authors and Affiliations

  1. Department of Marine Chemistry, Zhejiang Ocean University, Zhoushan, China

    Qiao Yang & Xiao-ling Zhang

  2. National Engineering Research Center for Marine Aquaculture, Zhoushan, China

    Ya-ming Ge

  3. Malaysia Genome Institute, National Institute of Biotechnology Malaysia, Kajang, Malaysia

    Nurhezreen Md Iqbal

  4. Institute of Animal Science, Guangdong Academy of Agricultural Sciences, Guangzhou, China

    Xi Yang

  5. ABI Group of GPM Project, Zhejiang Ocean University, Zhoushan, China

    Qiao Yang

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  1. Qiao Yang
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  4. Xi Yang
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Contributions

QY and XLZ conceived the project and designed the experiments; QY and YMG performed the experiments; QY, NMI, XY and XLZ analyzed the data; QY and XZ drafted and revised the manuscript. All authors have read and approved the final version of the manuscript.

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Correspondence to Xiao-ling Zhang.

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The DDBJ/EMBL/GenBank accession numbers for 16S rRNA gene sequences of the strain AM1-D1T is MH197128. The complete genome sequences of strain AM1-D1T have been deposited at DDBJ/EMBL/GenBank under the accession numbers CP018076 to CP018081 for its circular chromosome and five circular plasmids, respectively.

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Yang, Q., Ge, Ym., Iqbal, N.M. et al. Sulfitobacter alexandrii sp. nov., a new microalgae growth-promoting bacterium with exopolysaccharides bioflocculanting potential isolated from marine phycosphere. Antonie van Leeuwenhoek 114, 1091–1106 (2021). https://doi.org/10.1007/s10482-021-01580-0

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