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Research Article | Host-Microbe Biology

Host-Microbe Interactions in the Chemosynthetic Riftia pachyptila Symbiosis

Tjorven Hinzke, Manuel Kleiner, Corinna Breusing, Horst Felbeck, Robert Häsler, Stefan M. Sievert, Rabea Schlüter, Philip Rosenstiel, Thorsten B. H. Reusch, Thomas Schweder, Stephanie Markert
Daniel Distel, Invited Editor, Edward G. Ruby, Editor
Tjorven Hinzke
aInstitute of Marine Biotechnology e.V., Greifswald, Germany
bInstitute of Pharmacy, Department of Pharmaceutical Biotechnology, University of Greifswald, Greifswald, Germany
cEnergy Bioengineering Group, University of Calgary, Calgary, Canada
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  • ORCID record for Tjorven Hinzke
Manuel Kleiner
cEnergy Bioengineering Group, University of Calgary, Calgary, Canada
dDepartment of Plant & Microbial Biology, North Carolina State University, Raleigh, North Carolina, USA
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Corinna Breusing
eMonterey Bay Aquarium Research Institute, Moss Landing, California, USA
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Horst Felbeck
fScripps Institution of Oceanography, University of California San Diego, San Diego, California, USA
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Robert Häsler
gInstitute of Clinical Molecular Biology (IKMB), Kiel University, Kiel, Germany
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Stefan M. Sievert
hBiology Department, Woods Hole Oceanographic Institution, Woods Hole, Massachusetts, USA
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Rabea Schlüter
iImaging Center of the Department of Biology, University of Greifswald, Greifswald, Germany
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Philip Rosenstiel
gInstitute of Clinical Molecular Biology (IKMB), Kiel University, Kiel, Germany
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Thorsten B. H. Reusch
jMarine Evolutionary Ecology, GEOMAR Helmholtz Centre for Ocean Research Kiel, Kiel, Germany
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  • ORCID record for Thorsten B. H. Reusch
Thomas Schweder
aInstitute of Marine Biotechnology e.V., Greifswald, Germany
bInstitute of Pharmacy, Department of Pharmaceutical Biotechnology, University of Greifswald, Greifswald, Germany
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Stephanie Markert
aInstitute of Marine Biotechnology e.V., Greifswald, Germany
bInstitute of Pharmacy, Department of Pharmaceutical Biotechnology, University of Greifswald, Greifswald, Germany
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Daniel Distel
Northeastern University
Roles: Invited Editor
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Edward G. Ruby
University of Hawaii at Manoa
Roles: Editor
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DOI: 10.1128/mBio.02243-19
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  • FIG 1
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    FIG 1

    Main interactions in the Riftia symbiosis. "HOST" refers to processes in Riftia host tissues, while "SYMBIONT" refers to processes in the bacterial endosymbiont. A plus sign indicates presumably stimulating interactions, and a minus sign indicates presumably inhibiting interactions. For example, host efforts that protect the symbiont population from oxidative stress, i.e., ROS detoxification and fermentative metabolism (on the right), can promote symbiont biomass production (+). In contrast, host immune system-related proteins and antimicrobial peptides (AMPs) may inhibit symbiont biomass production (−). Circles, where present, indicate that the respective proteins are more abundant in S-rich (energy-rich) specimens (light circles) or S-depleted (energy-limited) specimens (dark circles). The dashed arrow indicates putative transfer of small organic compounds "Milking"; see Text S1, section 3).

  • FIG 2
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    FIG 2

    Functional groups of selected Riftia host proteins and their relative abundances in tissue samples. The heatmap shows log-normalized, centered, and scaled protein abundances. The bar chart shows summed abundances in %orgNSAF (percent normalized spectral abundance factor per organism, i.e., of all host proteins) of all proteins in the respective category. Error bars indicate standard error of the mean. Note the different scaling in the right part of the x axis. The “Chaperones, heat shock proteins” category also includes chaperonins and Clp proteases. FIH, factor inhibiting hypoxia-inducible factor 1α. S-depl, S depleted. Vest, vestimentum. Troph, trophosome. For a list of all identified proteins and their abundances, see Table S1a. (Categories presented in this figure are labeled with X in Table S1a in the column labeled Figure 2. The table can be filtered for these categories.)

  • FIG 3
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    FIG 3

    Transmission electron micrograph of a Riftia trophosome tissue section. Within the lobular trophosome tissue, this section shows the median and peripheral zones of an individual lobule with host bacteriocytes containing intracellular coccoid symbionts (S) located in dedicated vesicles (arrowheads, bacteriocyte membrane; double arrowheads, vesicle membrane). While the lower left area of the image shows mostly intact symbiont cells, arrows in the central area point to symbiont cells in the state of digestion by the host, where cell degradation is indicated by the presence of lamellar bodies. Image brightness and contrast were adjusted for visual clarity. Scale bar, 10 μm.

  • FIG 4
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    FIG 4

    Main nitrogen metabolic pathways in Riftia symbiosis. AGGP reductase, N-acetyl-gamma-glutamyl-phosphate reductase; CAD protein, multifunctional carbamoyl-phosphate synthetase 2, aspartate transcarbamoylase, and dihydroorotase protein; MTA, 5′-methylthioadenosine. Note that the symbiont might also be capable of nitrate respiration (25, 60), which is not depicted here.

  • FIG 5
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    FIG 5

    Selected domains with eukaryote-like structures and with putative functions in symbiont-host interactions in the Riftia symbiont and in selected other organisms and metagenomes. Color scale shows the percentage of genes/proteins containing the respective domain relative to all gene/protein sequences in this organism or metagenome. Numbers indicate the total number of genes/proteins containing the respective domain. For an overview of all analyzed organisms and domains, see Text S1, Fig. S5. For details on the organisms and communities, see Table S1d. The vent metagenome was sampled from hydrothermal vent fluid at a diffuse-flow vent site (Crab Spa) (137), which also houses Riftia. For further information about the selected protein groups, see Table S2. Riftia pachyptila endosymbiont metaproteome refers to the Riftia symbiont proteins detected in this study.

  • FIG 6
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    FIG 6

    Percent proteinaceous biomass contributions of host and symbiont as calculated from the share of host and symbiont spectral counts in all spectral counts of the respective samples (127; see Materials and Methods for details). Boldface lines indicate the means, and semitransparent areas indicate standard error of the mean. Sym, symbiont; S-depl, S depleted.

Tables

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  • TABLE 1

    Proteins which are putatively involved in symbiont digestion and which had significantly higher abundances in trophosome samples than in other tissues of S-rich and S-depleted specimens

    TABLE 1
    • ↵a Sig, Significance (x, significant; o, nonsignificant; false discovery rate, 0.05); troph, trophosome; S-depl, S depleted.

    • ↵b Subcellular localization (M, membrane-associated; S, secreted) was predicted using Phobius, TMHMM, and SignalP. Possibly M or S indicates localization prediction based on one tool only.

Supplemental Material

  • Figures
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  • Text S1

    Supplementary Results and Discussion with supplemental figures. Download Text S1, PDF file, 1.9 MB.

    Copyright © 2019 Hinzke et al.

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

  • Table S1

    (a) All Riftia host proteins identified in this study. (b) Potential autophagy-related Riftia proteins. (c) Potential Riftia antimicrobial peptides. (d) Genomes and metagenomes used for SMART analysis of eukaryote-like protein structures. (e) Sampling dates, cruise number, and number of biological replicates of Riftia samples used in this study. (f) Number of proteins with significant abundance differences in pairwise comparisons of Riftia tissues. (g) All Riftia symbiont proteins identified in this study. (h) Hemerythrin and myohemerythrin isoforms in Riftia and other invertebrates used for alignment in Text S1, Fig. S3. (i) Carbonic anhydrase isoforms in Riftia as detected in this study and described in the literature. Download Table S1, XLSX file, 1.8 MB.

    Copyright © 2019 Hinzke et al.

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

  • TABLE S2

    Domains and protein families with a putative role in host-symbiont interactions. Download Table S2, PDF file, 0.4 MB.

    Copyright © 2019 Hinzke et al.

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

  • TABLE S3

    Transcriptome completeness for the four different Riftia transcriptome assemblies based on the BUSCO eukaryote and metazoan datasets. Download Table S3, PDF file, 0.3 MB.

    Copyright © 2019 Hinzke et al.

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

  • TABLE S4

    Tools used to characterize Riftia host and symbiont proteins included in the combined Riftia host and symbiont database used in this study. Download Table S4, PDF file, 0.4 MB.

    Copyright © 2019 Hinzke et al.

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

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Host-Microbe Interactions in the Chemosynthetic Riftia pachyptila Symbiosis
Tjorven Hinzke, Manuel Kleiner, Corinna Breusing, Horst Felbeck, Robert Häsler, Stefan M. Sievert, Rabea Schlüter, Philip Rosenstiel, Thorsten B. H. Reusch, Thomas Schweder, Stephanie Markert
mBio Dec 2019, 10 (6) e02243-19; DOI: 10.1128/mBio.02243-19

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Host-Microbe Interactions in the Chemosynthetic Riftia pachyptila Symbiosis
Tjorven Hinzke, Manuel Kleiner, Corinna Breusing, Horst Felbeck, Robert Häsler, Stefan M. Sievert, Rabea Schlüter, Philip Rosenstiel, Thorsten B. H. Reusch, Thomas Schweder, Stephanie Markert
mBio Dec 2019, 10 (6) e02243-19; DOI: 10.1128/mBio.02243-19
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    • ABSTRACT
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KEYWORDS

host-microbe interactions
symbiosis
holobiont
chemosynthesis
hydrothermal vents
metaproteomics

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