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Title: Cooccurring Activities of Two Autotrophic Pathways in Symbionts of the Hydrothermal Vent Tubeworm Riftia pachyptila
ABSTRACT Genome and proteome data predict the presence of both the reductive citric acid cycle (rCAC; also called the reductive tricarboxylic acid cycle) and the Calvin-Benson-Bassham cycle (CBB) in “ Candidatus Endoriftia persephonae,” the autotrophic sulfur-oxidizing bacterial endosymbiont from the giant hydrothermal vent tubeworm Riftia pachyptila . We tested whether these cycles were differentially induced by sulfide supply, since the synthesis of biosynthetic intermediates by the rCAC is less energetically expensive than that by the CBB. R. pachyptila was incubated under in situ conditions in high-pressure aquaria under low (28 to 40 μmol · h −1 ) or high (180 to 276 μmol · h −1 ) rates of sulfide supply. Symbiont-bearing trophosome samples excised from R. pachyptila maintained under the two conditions were capable of similar rates of CO 2 fixation. Activities of the rCAC enzyme ATP-dependent citrate lyase (ACL) and the CBB enzyme 1,3-bisphosphate carboxylase/oxygenase (RubisCO) did not differ between the two conditions, although transcript abundances for ATP-dependent citrate lyase were 4- to 5-fold higher under low-sulfide conditions. δ 13 C values of internal dissolved inorganic carbon (DIC) pools were varied and did not correlate with sulfide supply rate. In samples taken from freshly collected R. pachyptila , δ 13 C values of lipids fell between those collected for organisms using either the rCAC or the CBB exclusively. These observations are consistent with cooccurring activities of the rCAC and the CBB in this symbiosis. IMPORTANCE Previous to this study, the activities of the rCAC and CBB in R. pachyptila had largely been inferred from “omics” studies of R. pachyptila without direct assessment of in situ conditions prior to collection. In this study, R. pachyptila was maintained and monitored in high-pressure aquaria prior to measuring its CO 2 fixation parameters. Results suggest that ranges in sulfide concentrations similar to those experienced in situ do not exert a strong influence on the relative activities of the rCAC and the CBB. This observation highlights the importance of further study of this symbiosis and other organisms with multiple CO 2 -fixing pathways, which recent genomics and biochemical studies suggest are likely to be more prevalent than anticipated.  more » « less
Award ID(s):
1952676
NSF-PAR ID:
10300376
Author(s) / Creator(s):
; ; ; ; ; ; ; ;
Editor(s):
Atomi, Haruyuki
Date Published:
Journal Name:
Applied and Environmental Microbiology
Volume:
87
Issue:
17
ISSN:
0099-2240
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
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  1. Summary

    RubisCO, the CO2fixing enzyme of the Calvin–Benson–Bassham (CBB) cycle, is responsible for the majority of carbon fixation on Earth. RubisCO fixes12CO2faster than13CO2resulting in13C‐depleted biomass, enabling the use of δ13C values to trace CBB activity in contemporary and ancient environments. Enzymatic fractionation is expressed as anεvalue, and is routinely used in modelling, for example, the global carbon cycle and climate change, and for interpreting trophic interactions. Although values for spinach RubisCO (ε= ~29‰) have routinely been used in such efforts, there are five different forms of RubisCO utilized by diverse photolithoautotrophs and chemolithoautotrophs andεvalues, now known for four forms (IA, B, D and II), vary substantially withε =11‰ to 27‰. Given the importance ofεvalues in δ13C evaluation, we measured enzymatic fractionation of the fifth form, form IC RubisCO, which is found widely in aquatic and terrestrial environments. Values were determined for two model organisms, the ‘Proteobacteria’ Ralstonia eutropha (ε= 19.0‰) andRhodobacter sphaeroides(ε =22.4‰). It is apparent from these measurements that all RubisCO forms measured to date discriminate less than commonly assumed based on spinach, and that enzymeεvalues must be considered when interpreting and modelling variability of δ13C values in nature.

     
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  2. Bose, Arpita (Ed.)
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Retrieved from https://par.nsf.gov/biblio/10300376. <em>Applied and Environmental Microbiology</em> 87.17 Web. doi:10.1128/AEM.00794-21. </div> <div class="modal-footer"> <button class="btn btn-sm btn-default" data-dismiss="modal" aria-hidden="true">Close</button> </div> </div> </div> </div></li> <li class="links-format"><a href="#cite-apa" data-toggle="modal">APA</a> <div id="cite-apa" class="modal" tabindex="-1" role="dialog" aria-labelledby="cite-apa_label" aria-hidden="true"> <div class="modal-dialog"> <div class="modal-content"> <div class="modal-header"> <button type="button" class="close" data-dismiss="modal" aria-hidden="true">×</button> <strong id="cite-apa_label">Cite: APA Format</strong> </div> <div class="modal-body">Leonard, Juliana M., Mitchell, Jessica, Beinart, Roxanne A., Delaney, Jennifer A., Sanders, Jon G., Ellis, Greg, Goddard, Ethan A., Girguis, Peter R., & Scott, Kathleen M. <em>Cooccurring Activities of Two Autotrophic Pathways in Symbionts of the Hydrothermal Vent Tubeworm Riftia pachyptila</em>. <em>Applied and Environmental Microbiology</em>, <em>87</em> (17). Retrieved from https://par.nsf.gov/biblio/10300376. <a href="https://doi.org/10.1128/AEM.00794-21">https://doi.org/10.1128/AEM.00794-21</a> </div> <div class="modal-footer"> <button class="btn btn-sm btn-default" data-dismiss="modal" aria-hidden="true">Close</button> </div> </div> </div> </div></li> <li class="links-format"><a href="#cite-chi" data-toggle="modal">Chicago</a> <div id="cite-chi" class="modal" tabindex="-1" role="dialog" aria-labelledby="cite-chi_label" aria-hidden="true"> <div class="modal-dialog"> <div class="modal-content"> <div class="modal-header"> <button type="button" class="close" data-dismiss="modal" aria-hidden="true">×</button> <strong id="cite-chi_label">Cite: Chicago Format</strong> </div> <div class="modal-body">Leonard, Juliana M., Mitchell, Jessica, Beinart, Roxanne A., Delaney, Jennifer A., Sanders, Jon G., Ellis, Greg, Goddard, Ethan A., Girguis, Peter R., and Scott, Kathleen M. "Cooccurring Activities of Two Autotrophic Pathways in Symbionts of the Hydrothermal Vent Tubeworm Riftia pachyptila". <em>Applied and Environmental Microbiology</em> 87 (17). Country unknown/Code not available. <a href="https://doi.org/10.1128/AEM.00794-21">https://doi.org/10.1128/AEM.00794-21.</a> <a href="https://par.nsf.gov/biblio/10300376">https://par.nsf.gov/biblio/10300376</a>. </div> <div class="modal-footer"> <button class="btn btn-sm btn-default" data-dismiss="modal" aria-hidden="true">Close</button> </div> </div> </div> </div></li> <li class="links-format"><a href="#cite-bib" data-toggle="modal">BibTeX</a> <div id="cite-bib" class="modal" tabindex="-1" role="dialog" aria-labelledby="cite-bib_label" aria-hidden="true"> <div class="modal-dialog"> <div class="modal-content"> <div class="modal-header"> <button type="button" class="close" data-dismiss="modal" aria-hidden="true">×</button> <strong id="cite-bib_label">Cite: BibTeX Format</strong> </div> <div class="modal-body"> @article{osti_10300376,<br/> place = {Country unknown/Code not available}, title = {Cooccurring Activities of Two Autotrophic Pathways in Symbionts of the Hydrothermal Vent Tubeworm Riftia pachyptila}, url = {https://par.nsf.gov/biblio/10300376}, DOI = {10.1128/AEM.00794-21}, abstractNote = {ABSTRACT Genome and proteome data predict the presence of both the reductive citric acid cycle (rCAC; also called the reductive tricarboxylic acid cycle) and the Calvin-Benson-Bassham cycle (CBB) in “ Candidatus Endoriftia persephonae,” the autotrophic sulfur-oxidizing bacterial endosymbiont from the giant hydrothermal vent tubeworm Riftia pachyptila . We tested whether these cycles were differentially induced by sulfide supply, since the synthesis of biosynthetic intermediates by the rCAC is less energetically expensive than that by the CBB. R. pachyptila was incubated under in situ conditions in high-pressure aquaria under low (28 to 40 μmol · h −1 ) or high (180 to 276 μmol · h −1 ) rates of sulfide supply. Symbiont-bearing trophosome samples excised from R. pachyptila maintained under the two conditions were capable of similar rates of CO 2 fixation. Activities of the rCAC enzyme ATP-dependent citrate lyase (ACL) and the CBB enzyme 1,3-bisphosphate carboxylase/oxygenase (RubisCO) did not differ between the two conditions, although transcript abundances for ATP-dependent citrate lyase were 4- to 5-fold higher under low-sulfide conditions. δ 13 C values of internal dissolved inorganic carbon (DIC) pools were varied and did not correlate with sulfide supply rate. In samples taken from freshly collected R. pachyptila , δ 13 C values of lipids fell between those collected for organisms using either the rCAC or the CBB exclusively. These observations are consistent with cooccurring activities of the rCAC and the CBB in this symbiosis. IMPORTANCE Previous to this study, the activities of the rCAC and CBB in R. pachyptila had largely been inferred from “omics” studies of R. pachyptila without direct assessment of in situ conditions prior to collection. In this study, R. pachyptila was maintained and monitored in high-pressure aquaria prior to measuring its CO 2 fixation parameters. Results suggest that ranges in sulfide concentrations similar to those experienced in situ do not exert a strong influence on the relative activities of the rCAC and the CBB. This observation highlights the importance of further study of this symbiosis and other organisms with multiple CO 2 -fixing pathways, which recent genomics and biochemical studies suggest are likely to be more prevalent than anticipated.}, journal = {Applied and Environmental Microbiology}, volume = {87}, number = {17}, author = {Leonard, Juliana M. and Mitchell, Jessica and Beinart, Roxanne A. and Delaney, Jennifer A. and Sanders, Jon G. and Ellis, Greg and Goddard, Ethan A. and Girguis, Peter R. and Scott, Kathleen M.}, editor = {Atomi, Haruyuki} }</div> <div class="modal-footer"> <button class="btn btn-sm btn-default" data-dismiss="modal" aria-hidden="true">Close</button> </div> </div> </div> </div></li> <li class="divider"></li> </ul> <ul class="nav nav-list" style="font-size: 14px; font-family: Arial Regular;"> <li class="nav-header header-format">Export Metadata</li> <li class="links-format"><a href="https://par.nsf.gov/endnote?osti_id=10300376">EndNote</a></li> <li class="links-format"><a href="https://par.nsf.gov/export/format:excel/osti-id:10300376">Excel</a></li> <li class="links-format"><a href="https://par.nsf.gov/export/format:csv/osti-id:10300376">CSV</a></li> <li class="links-format"><a href="https://par.nsf.gov/export/format:xml/osti-id:10300376">XML</a></li> <li class="divider"></li> </ul> <ul class="nav nav-list" style="font-size: 14px; 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