Coastal Transient Niches Shape the Microdiversity Pattern of a Bacterioplankton Population with Reduced Genomes

Chu, Xiao; Wang, Xiaojun; Cheung, Lok Shan; Feng, Xiaoyuan; Ang, Put O.; Lee, Joe; Crowe, Sean A.; Luo, Haiwei

doi:10.1128/mbio.00571-22

Cited by 6 publications

(7 citation statements)

References 87 publications

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“…S7). This is unexpected, since in the model pelagic bacterium Ruegeria pomeroyi DSS-3, the cbb 3 -type cytochrome c oxidase is likely to be responsible for the exceptionally high affinity for oxygen and efficient oxygen consumption at nanomolar scales in this organism (Chu et al, 2022). However, cbb 3 -type cytochrome c oxidase may have other functions.…”

Section: Resultsmentioning

confidence: 99%

Sulfur oxidation through rDsr in a novel Sox-free marine Roseobacter lineage

Lin,

Feng,

Wang

et al. 2024

Preprint

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Sulfur oxidation is an essential biogeochemical process in coastal sediments. Of the two typical sulfur-oxidizing metabolic pathways, the reverse dissimilatory sulfite reductase pathway (rDsr) is recognized for its superior energy conservation efficiency compared to the Sox multi-enzyme system and thus might be important in intertidal habitats where electron acceptors are periodically limited. Here, we isolated 10 intertidal sediment strains that compose a novelRuegerialineage in the globally abundant marine Roseobacter group. They possess a complete rDsr pathway but lack the entire Sox system, whereas all known sulfur-oxidizing Roseobacters rely on Sox. In fact, rDsr-carrying but Sox-free bacteria are rare among all sequenced bacterial genomes (only 20 out of 35798), and how sulfur oxidation is driven exclusively by rDsr has not been investigated. Physiological assays, sulfur intermediate measurements, and transcriptomic analyses reveal that rDsr activation in thisRuegerialineage occurs exclusively under microaerobic conditions and is coupled with thiosulfate oxidation in tandem with denitrification. Metagenomic analysis shows that rDsr sequences are enriched in marine habitats characterized by oxygen depletion, consistent with our physiological data. Further, theRhodobacteralesorder whereRuegeriabelongs accounts for approximately 5% of the rDsr-bearing bacterial community in intertidal sediments globally, underscoring its significant role in sulfur oxidation in this important marine environment.

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Section: Resultsmentioning

confidence: 99%

Sulfur oxidation through rDsr in a novel Sox-free marine Roseobacter lineage

Lin,

Feng,

Wang

et al. 2024

Preprint

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“…As mentioned above, PopCOGenT assesses population structure by inferring the extent of recombination relative to the amount of divergence between genomes and this in turn can help determine where natural genetic boundaries exist between strains [ 27 ]. PopCOGenT has been used to distinguish recent gene flow events from historical ones and to identify ancestral nodes in phylogenomic trees that lead to speciation events [ 53 ]. PopCOGenT can be used to predict the recombination pattern and population structure within bacterial species and reveal distinct populations.…”

Section: Discussionmentioning

confidence: 99%

Genome sequencing and multifaceted taxonomic analysis of novel strains of violacein-producing bacteria and non-violacein-producing close relatives

et al. 2023

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Violacein is a water-insoluble violet pigment produced by various Gram-negative bacteria. The compound and the bacteria that produce it have been gaining attention due to the antimicrobial and proposed antitumour properties of violacein and the possibility that strains producing it may have broad industrial uses. Bacteria that produce violacein have been isolated from diverse environments including fresh and ocean waters, glaciers, tropical soils, trees, fish and the skin of amphibians. We report here the isolation and characterization of six violacein-producing bacterial strains and three non-violacein-producing close relatives, each isolated from either an aquatic environment or moist food materials in northern California, USA. For each isolate, we characterized traditional phenotypes, generated and analysed draft genome sequences, and carried out multiple types of taxonomic, phylogenetic and phylogenomic analyses. Based on these analyses we assign putative identifications to the nine isolates, which include representatives of the genera Chromobacterium , Aquitalea , Iodobacter , Duganella , Massilia and Janthinobacterium . In addition, we discuss the utility of various metrics for taxonomic assignment in these groups including average nucleotide identity, whole genome phylogenetic analysis and extent of recent homologous recombination using the software program PopCOGenT.

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“…It was shown to outperform earlier methods and was used to delineate population boundaries of many prokaryotic species for N e estimation 12 . We therefore used PopCOGenT to delineate populations for CHUG based on the published genomes of 39 isolates we sampled mostly from brown algae ambient seawater 25,26 as well as newly sequenced genomes of seven isolates from more diverse marine ecosystems such as regular coastal seawater and coral ambient seawater (Fig. S2).…”

Section: Genome Sizes Of the Roseobacter Group Members From Surface O...mentioning

confidence: 99%

“…Early community structure analyses based on 16S rRNA gene revealed that marine Roseobacter communities are dominated by a few uncultivated lineages 17 , whose genomes are becoming increasingly available through sequencing novel cultured members and sequencing uncultured members by single-cell genomics and metagenomic binning. Classical examples are DC5-80-3 (also named RCA or Planktomarina) [18][19][20][21] , CHAB-I-5 15,22 , ChesI-A/B (also named SAG-O19) 23 , NAC11-7 24 , and more recently CHUG 25,26 . These lineages constitute a polyphyletic group in the phylogenomic tree but form a tight pelagic Roseobacter cluster (PRC) in a dendrogram clustered from the presence and absence of gene families, reflecting their convergent evolution towards shared genome content and reduced genome sizes 22,26 .…”

Section: Introductionmentioning

confidence: 99%

“…The copyright holder for this preprint this version posted February 4, 2024. ; https://doi.org/10.1101/2024.02.04.578831 doi: bioRxiv preprint 21 , CHAB-I-5 15,22 , ChesI-A/B (also named SAG-O19) 23 , NAC11-7 24 , and more recently CHUG 25,26 . These lineages constitute a polyphyletic group in the phylogenomic tree but form a tight pelagic Roseobacter cluster (PRC) in a dendrogram clustered from the presence and absence of gene families, reflecting their convergent evolution towards shared genome content and reduced genome sizes 22,26 .…”

Section: Introductionmentioning

confidence: 99%

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A neutral process of genome reduction in marine bacterioplankton

Wang,

Xie,

et al. 2024

Preprint

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Marine bacterioplankton communities are dominated by cells equipped with small genomes. Streamlining selection has been accepted as the main force driving their genome reduction. Here, we report that a neutral evolutionary mechanism governs genome reduction in the Roseobacter group that represents 5-20% of the bacterioplankton cells in coastal waters. Using representative strains that fall into three genome size groups (2-3, 3-4, and 4-5 Mbp), we measured their genomic mutation rates (μ) through long-term mutation accumulation experiments followed by genome sequencing the resulting 437 mutant lines. We further calculated their effective population sizes (Ne) based on μ and the neutral genetic diversity of the studied species, the latter estimated based on multiple genome sequences of natural isolates collected from global oceans with their population structure considered. A surprising finding is that Ne scales positively with genome size, which is the opposite of the expectation from the streamlining selection theory. As the strength of random genetic drift is the inverse of Ne, this result instead suggests drift as the primary driver of genome reduction. Additionally, we report a negative scaling between μ and genome size, which is the first experimental evidence for the long-lasting hypothesis that mutation rate increases play a part in marine bacterial genome reduction. As μ scales inversely with Ne, genetic drift appears to be the ultimate cause of genome reduction in these Roseobacters. Our finding discounts, but is insufficient to reject, the streamlining theory because streamlining process is expected to be more effective in oligotrophic open ocean waters.

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Coastal Transient Niches Shape the Microdiversity Pattern of a Bacterioplankton Population with Reduced Genomes

Cited by 6 publications

References 87 publications

Sulfur oxidation through rDsr in a novel Sox-free marine Roseobacter lineage

Sulfur oxidation through rDsr in a novel Sox-free marine Roseobacter lineage

Genome sequencing and multifaceted taxonomic analysis of novel strains of violacein-producing bacteria and non-violacein-producing close relatives

A neutral process of genome reduction in marine bacterioplankton

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