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Editor's Pick Research Article | Ecological and Evolutionary Science

Unique Patterns and Biogeochemical Relevance of Two-Component Sensing in Marine Bacteria

Noelle A. Held, Matthew R. McIlvin, Dawn M. Moran, Michael T. Laub, Mak A. Saito
Olivia Mason, Editor
Noelle A. Held
MIT-WHOI Joint Program in Oceanography/Applied Ocean Science and Engineering, Woods Hole, Massachusetts, USA
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Matthew R. McIlvin
Marine Chemistry and Geochemistry Department, Woods Hole Oceanographic Institution, Woods Hole, Massachusetts, USA
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Dawn M. Moran
Marine Chemistry and Geochemistry Department, Woods Hole Oceanographic Institution, Woods Hole, Massachusetts, USA
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Michael T. Laub
Department of Biology, Massachusetts Institute of Technology, Cambridge, Massachusetts, USAHoward Hughes Medical Institute, Massachusetts Institute of Technology, Cambridge, Massachusetts, USA
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Mak A. Saito
Marine Chemistry and Geochemistry Department, Woods Hole Oceanographic Institution, Woods Hole, Massachusetts, USA
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Olivia Mason
Florida State University
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DOI: 10.1128/mSystems.00317-18
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  • FIG 1
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    FIG 1

    Overview of two-component-system signaling in (A) a traditional histidine kinase-response regulator system and (B) a hybrid histidine kinase system. In panel A, the phosphorylation is transferred from the histidine kinase to the response regulator by a direct protein-protein interaction. In panel B, the phosphorylation is transferred to an internal receiver domain on the histidine kinase, then to one or more histidine phosphotransfer (Hpt) proteins, and finally to the terminal response regulator.

  • FIG 2
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    FIG 2

    Number of histidine kinase sensory genes in the genomes of 328 diverse marine bacterial species (scale indicated by concentric circles). Phylogenetic groups of interest are delineated by color. The number of histidine kinases in the data set ranges from 1 (Pelagibacter) to 174 (Desulfovibrio inopinatus DSM 10711).

  • FIG 3
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    FIG 3

    (A) K-means clustering of the number of histidine kinases (HPK) per 100 protein-encoding genes as a function of genome size. The dashed line represents the average, 0.902 histidine kinases per 100 protein-encoding genes in the genome. (B) The number of histidine kinases per 100 protein-encoding genes in the genome for organisms unambiguously designated copiotrophs or oligotrophs. Error bars represent 95% confidence intervals of the average value within the copiotroph (n = 74) and oligotroph (n = 34) categories. The copiotrophs were shown to have significantly more histidine kinases per gene than the oligotrophs by a Student's t test (P = 3e−15).

  • FIG 4
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    FIG 4

    (A) Number of response regulator (RR) genes versus histidine kinase (HPK) genes in marine (orange) and reference (blue) bacteria. The dotted black line represents a 1:1 relationship. When the number of TCS systems is low, the ratio of RRs to HPKs is approximately 1. When the number of two-component systems is large (50 or more), the RR-to-HPK ratio tends to be much lower than 1. (B) RR/HPK ratio of marine and reference bacteria. While the differences are subtle, the marine bacteria have a significantly larger RR/HPK ratio on average (1.03) than the reference bacteria (0.99) as shown by a one-tailed ANOVA test [P = 0.0095, F(327,1151) = 6.73].

  • FIG 5
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    FIG 5

    Distribution of TCS genes in various marine bacterial species. The genome is linearized and depicted as a number line; genes are represented as vertical lines based on their starting location. Histidine kinase genes and response regulator genes that are within four genes of another TCS gene are represented as long blue and green lines, respectively. Orphan histidine kinases and response regulators are represented as short cyan and red lines, respectively. There are many orphan TCS genes in marine bacteria, including in oligotrophs such as Pelagibacter and Prochlorococcus.

  • FIG 6
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    FIG 6

    Percentage of histidine kinases that are hybrids in marine (orange) and reference (blue) bacteria. The marine bacteria have a greater percentage of hybrid histidine kinases than the reference bacteria. Error bars represent a bootstrapped 95% confidence interval. The difference is statistically significant by a Student's t test (P = 3e−10).

  • FIG 7
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    FIG 7

    (A) Number of histidine kinases per 100 protein-encoding genes and (B) RR/HPK ratio of Proteobacteria. (C) Number of histidine kinases per 100 protein-encoding genes and (D) RR/HPK ratio of Cyanobacteria. Proteobacteria, in particular the Deltaproteobacteria, have many histidine kinases per gene compared with the Cyanobacteria. The RR/HPK ratio of the Proteobacteria tends to be greater than 1. Note that Crocosphaera, Synechococcus, and Trichodesmium have more histidine kinases per 100 protein-encoding genes than Prochlorococcus, which is adapted to highly oligotrophic conditions. The picocyanobacteria Prochlorococcus and Synechococcus have particularly high RR/HPK ratios.

  • FIG 8
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    FIG 8

    (A) Distribution of response regulator PMT9312_0717 in metaproteomes of the South Pacific Ocean. (B) Distribution of dissolved phosphate in the water column. (C) The abundance of PMT9312_0717 (measured as spectral counts) is correlated to phosphate concentrations. The relationship can be modeled by a power law. The distribution of Prochlorococcus cells is high across the transect (see Fig. S2). (D) Map of the METZYME transect where these samples were acquired. (E) Taxonomic information for the identified peptides. Two peptides were identified, one of which was annotated separately to two different Prochlorococcus strains. METATRYP analysis suggests that both of these peptides are specific to the order Synechococcales.

Tables

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  • TABLE 1

    Characteristics of copiotrophs versus oligotrophs and their TCS system genesa

    GenusExample
    genome
    size (bp)
    Example %
    growth rate
    (per day)
    Lifestyle(s)HPK/100
    genes
    RR/HPK
    ratio
    % hybrid
    HPKs
    Reference
    Pelagibacter1,200–1,4000.4–0.58Oligotroph0.3870.83Typically 059
    Prochlorococcus1,200–2,0000.51–0.83Oligotroph0.761.22Typically 060
    Synechococcus1,500–3,0001Oligotroph1.0051.230–4060
    Trichodesmium∼5,0000.29Oligotroph0.6940.75315–3561
    Crocosphaera∼6,0000.5Oligotroph0.7230.992∼3562
    Roseobacter∼5,0001.45Varies/copiotroph0.7550.99110–4063
    Vibrio∼5,000Up to 14.3Copiotroph1.251.0725–5064
    Alteromonas4,000–4,5006Copiotroph1.431.06∼4065
    Pseudoalteromonas3,000–5,000∼30Copiotroph1.51.140–5066
    • ↵a HPK, histidine kinase; RR, response regulator.

Supplemental Material

  • Figures
  • Tables
  • TABLE S1

    TCS gene data for the 328 marine bacteria surveyed, including taxonomic information for each genome. Download Table S1, XLSX file, 0.2 MB.

    Copyright © 2019 Held et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • FIG S1

    Phylogenetic breakdown of the marine and reference data sets, showing the diversity of the genomes used in this analysis. Download FIG S1, EPS file, 0.09 MB.

    Copyright © 2019 Held et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • TABLE S2

    TCS gene data for the 1,152 reference bacteria, including taxonomic information for each genome. Download Table S2, XLSX file, 0.2 MB.

    Copyright © 2019 Held et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • FIG S2

    Hydrographic and pigment data from the METZYME cruise. The distribution of PMT9312_0717 is not well correlated with chlorophyll-a, divinyl chlorophyll-a, temperature, nor salinity in this region but is well correlated with dissolved-phosphate concentrations (see Fig. 8). Data are from M. Saito, Biological and Chemical Oceanography Data Management Office (BCO-DMO), https://www.bco-dmo.org/dataset-deployment/716688 (data set version 11 October 2017; accessed 26 October 2018), and M. Saito, Biological and Chemical Oceanography Data Management Office (BCO-DMO), https://www.bco-dmo.org/dataset-deployment/646117 (data set version 1 August 2017; accessed 26 October 2018). Download FIG S2, EPS file, 1.0 MB.

    Copyright © 2019 Held et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

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Unique Patterns and Biogeochemical Relevance of Two-Component Sensing in Marine Bacteria
Noelle A. Held, Matthew R. McIlvin, Dawn M. Moran, Michael T. Laub, Mak A. Saito
mSystems Feb 2019, 4 (1) e00317-18; DOI: 10.1128/mSystems.00317-18

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Unique Patterns and Biogeochemical Relevance of Two-Component Sensing in Marine Bacteria
Noelle A. Held, Matthew R. McIlvin, Dawn M. Moran, Michael T. Laub, Mak A. Saito
mSystems Feb 2019, 4 (1) e00317-18; DOI: 10.1128/mSystems.00317-18
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    • ABSTRACT
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KEYWORDS

biogeochemistry
cell signaling
gene regulation
marine microbiology
proteomics
regulatory network
two-component system

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