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Revisiting the taxonomy of the genus Rhodopirellula with the proposal for reclassification of the genus to Rhodopirellula sensu stricto, Aporhodopirellula gen. nov., Allorhodopirellula gen. nov. and Neorhodopirellula gen. nov

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Abstract

The current genus Rhodopirellula consists of marine bacteria which belong to the family Pirellulaceae of the phylum Planctomycetota. Members of the genus Rhodopirellula are aerobic, mesophiles and chemoheterotrophs. The here conducted analysis built on 16S rRNA gene sequence and multi-locus sequence analysis based phylogenomic trees suggested that the genus is subdivided into four clades. Existing Rhodopirellula species were studied extensively based on phenotypic, genomic and chemotaxonomic parameters. The heterogeneity was further confirmed by overall genome-related indices (OGRI) including digital DNA–DNA hybridization (dDDH), average nucleotide identity (ANI), average amino acid identity (AAI), and percentage of conserved proteins (POCP). AAI and POCP values between the clades of the genus Rhodopirellula were 62.2–69.6% and 49.5–62.5%, respectively. Comparative genomic approaches like pan-genome analysis and conserved signature indels (CSIs) also support the division of the clades. The genomic incoherence of the members of the genus is further supported by variations in phenotypic characteristics. Thus, with the here applied integrated comparative genomic and polyphasic approaches, we propose the reclassification of the genus Rhodopirellula to three new genera: Aporhodopirellula gen. nov., Allorhodopirellula gen. nov., and Neorhodopirellula gen. nov.

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Abbreviations

dDDH:

Digital DNA–DNA hybridization

gANI:

Genomic average nucleotide identity

AAI:

Average amino acid identity

POCP:

Percentage of conserved proteins

NCBI:

National Centre for Biotechnology Information

BLAST:

Basic Local Alignment Search Tool

JGI:

Joint Genome Institute

MUSCLE:

MUltiple Sequence Comparison by Log-Expectation

MEGA:

Molecular Evolutionary Genetics Analysis

UBCG:

Up-to-date Bacterial Core Gene set

BPGA:

Bacterial pangenome analysis

MLSA:

Multi-locus sequence analysis

DSMZ:

Deutsche Sammlung von Mikroorganismen und Zellkulturen GmbH

JCM:

Japan Collection of Microorganisms-RIKEN BioResource Center

NBRC:

NITE Biological Resource Center

LMG:

Laboratorium voor Microbiologie

CECT:

Colección Española de Cultivos Tipo

ITOL:

Interactive Tree Of Life

RAxML:

Randomized Axelerated Maximum Likelihood

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Acknowledgements

We are grateful to Prof. Bernhard Schink (University of Konstanz, Germany) and Prof. Aharon Oren (The Hebrew University of Jerusalem, Israel) for correcting the protologues. We thank Prof. Markus Göker (DOE-JGI, USA) for sharing the genome information. SPK thanks PMRF for a fellowship. AR and VL thank DST Inspire (JRF/SRF), RB thanks UGC JRF, and JU thanks TEQIP for fellowship. Ramana thanks the Department of Biotechnology, Government of India for the award of Tata Innovation Fellowship and IoE-UoH for project grant. Financial support received from CSIR is acknowledged. Infrastructural facilities funded by DST-FIST (UoH and JNTUH), UGC-SAP (DRS; UoH), TEQIP and AICTE (from JNTUH) are acknowledged.

Funding

The work was supported by the IoE-UoH project grant, Prime Minister Research Fellow (PMRF) Research grant, Council for Scientific and Industrial Research (38/(1470)/18/EMR-II).

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Contributions

SPK designed and planned the studies under the supervision of CS and CVR. SPK, AR, GS, and JU performed the genomic, phylogenetic analysis and functional annotations. VCA, VL, and BR performed the comparative genomic analysis. SPK wrote the manuscript. CVR and CS supervised the study, contributed to text preparation and revised the manuscript. All authors read and approved the final version of the manuscript.

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Correspondence to Chintalapati Sasikala or Chintalapati Venkata Ramana.

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Sreya, P., Suresh, G., Rai, A. et al. Revisiting the taxonomy of the genus Rhodopirellula with the proposal for reclassification of the genus to Rhodopirellula sensu stricto, Aporhodopirellula gen. nov., Allorhodopirellula gen. nov. and Neorhodopirellula gen. nov. Antonie van Leeuwenhoek 116, 243–264 (2023). https://doi.org/10.1007/s10482-022-01801-0

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