Cryptic speciation of a pelagic Roseobacter population varying at a few thousand nucleotide sites

Abstract

A drop of seawater contains numerous microspatial niches at the scale relevant to microbial activities. Examples are abiotic niches such as detrital particles that show different sizes and organic contents, and biotic niches resulting from bacteria–phage and bacteria–phytoplankton interactions. A common practice to investigate the impact of microenvironments on bacterial evolution is to separate the microenvironments physically and compare the bacterial inhabitants from each. It remains poorly understood, however, which microenvironment primarily drives bacterioplankton evolution in the pelagic ocean. By applying a dilution cultivation approach to an undisturbed coastal water sample, we isolate a bacterial population affiliated with the globally dominant Roseobacter group. Although varying at just a few thousand nucleotide sites across the whole genomes, members of this clonal population are diverging into two genetically separated subspecies. Genes underlying speciation are not unique to subspecies but instead clustered at the shared regions that represent ~6% of the genomic DNA. They are primarily involved in vitamin synthesis, motility, oxidative defense, carbohydrate, and amino acid utilization, consistent with the known strategies that roseobacters take to interact with phytoplankton and particles. Physiological assays corroborate that one subspecies outcompetes the other in these traits. Our results indicate that the microenvironments in the pelagic ocean represented by phytoplankton and organic particles are likely important niches that drive the cryptic speciation of the Roseobacter population, though microhabitats contributed by other less abundant pelagic hosts cannot be ruled out.

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Fig. 1: Differentiation of the Roseobacter population.
Fig. 2: The pangenome of the Roseobacter population.
Fig. 3: Phenotypic differentiation of the Clade R-I (represented by xm-d-517 and xm-m-339-2) and Clade R-II (represented by xm-v-204 and xm-m-314) of the Roseobacter population.

Data availability

Genomic sequences of the Roseobacter and Marinobacterium population are available at the NCBI GenBank database under the accession number WBXQ00000000-WBYV00000000.

Code availability

The scripts used for the population structure analyses, recombination history inference, SNP density plot and allelic replacements inference have been deposited in the online repository (https://github.com/Xiaojun928/Population-genomics).

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Acknowledgements

We thank Ying Sun for sharing her bioinformatics pipeline, Xiaoyuan Feng for his helpful discussion, Kan Zhu for his assistance in the access to the OmniLOG instrument, and Leon Zou (BiOLOG Inc.) for his helpful suggestions on the Biolog experiments. This work was supported by the National Key R&D Program of China (2018YFC0309800), the National Natural Science Foundation of China (41776129), the National Key R&D Program of China (2016YFA0601400 to YZ), the Shenzhen City Knowledge Innovation Plan (JCYJ20160530174441706 to AY), the Hong Kong Research Grants Council General Research Fund (14163917), the Hong Kong Environment and Conservation Fund (15/2016), the Hong Kong Research Grants Council Area of Excellence Scheme (AoE/M-403/16), and the Direct Grant of CUHK (4053257 & 3132809).

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Wang, X., Zhang, Y., Ren, M. et al. Cryptic speciation of a pelagic Roseobacter population varying at a few thousand nucleotide sites. ISME J (2020). https://doi.org/10.1038/s41396-020-00743-7

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