Torn apart and reunited: impact of a heterotroph on the transcriptome of Prochlorococcus

Microbial interactions, whether direct or indirect, profoundly affect the physiology of individual cells and ultimately have the potential to shape the biogeochemistry of the Earth. For example, the growth of Prochlorococcus, the numerically dominant cyanobacterium in the oceans, can be improved by...

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Main Authors: Biller, Steven, Coe, Allison, Chisholm, Sallie (Penny)
Other Authors: Massachusetts Institute of Technology. Department of Biology
Format: Article
Language:en_US
Published: Nature Publishing Group 2018
Online Access:http://hdl.handle.net/1721.1/119005
https://orcid.org/0000-0002-2638-823X
https://orcid.org/0000-0003-1480-2445
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author Biller, Steven
Coe, Allison
Chisholm, Sallie (Penny)
author2 Massachusetts Institute of Technology. Department of Biology
author_facet Massachusetts Institute of Technology. Department of Biology
Biller, Steven
Coe, Allison
Chisholm, Sallie (Penny)
author_sort Biller, Steven
collection MIT
description Microbial interactions, whether direct or indirect, profoundly affect the physiology of individual cells and ultimately have the potential to shape the biogeochemistry of the Earth. For example, the growth of Prochlorococcus, the numerically dominant cyanobacterium in the oceans, can be improved by the activity of co-occurring heterotrophs. This effect has been largely attributed to the role of heterotrophs in detoxifying reactive oxygen species that Prochlorococcus, which lacks catalase, cannot. Here, we explore this phenomenon further by examining how the entire transcriptome of Prochlorococcus NATL2A changes in the presence of a naturally co-occurring heterotroph, Alteromonas macleodii MIT1002, with which it was co-cultured for years, separated and then reunited. Significant changes in the Prochlorococcus transcriptome were evident within 6 h of initiating co-culture, with groups of transcripts changing in different temporal waves. Many transcriptional changes persisted throughout the 48 h experiment, suggesting that the presence of the heterotroph affected a stable shift in Prochlorococcus physiology. These initial transcriptome changes largely corresponded to reduced stress conditions for Prochlorococcus, as inferred from the depletion of transcripts encoding DNA repair enzymes and many members of the ‘high light inducible’ family of stress–response proteins. Later, notable changes were seen in transcripts encoding components of the photosynthetic apparatus (particularly, an increase in PSI subunits and chlorophyll synthesis enzymes), ribosomal proteins and biosynthetic enzymes, suggesting that the introduction of the heterotroph may have induced increased production of reduced carbon compounds for export. Changes in secretion-related proteins and transporters also highlight the potential for metabolic exchange between the two strains.
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spelling mit-1721.1/1190052022-10-01T10:58:21Z Torn apart and reunited: impact of a heterotroph on the transcriptome of Prochlorococcus Biller, Steven Coe, Allison Chisholm, Sallie (Penny) Massachusetts Institute of Technology. Department of Biology Sallie (Penny) Chisholm Biller, Steven Coe, Allison Chisholm, Sallie W Microbial interactions, whether direct or indirect, profoundly affect the physiology of individual cells and ultimately have the potential to shape the biogeochemistry of the Earth. For example, the growth of Prochlorococcus, the numerically dominant cyanobacterium in the oceans, can be improved by the activity of co-occurring heterotrophs. This effect has been largely attributed to the role of heterotrophs in detoxifying reactive oxygen species that Prochlorococcus, which lacks catalase, cannot. Here, we explore this phenomenon further by examining how the entire transcriptome of Prochlorococcus NATL2A changes in the presence of a naturally co-occurring heterotroph, Alteromonas macleodii MIT1002, with which it was co-cultured for years, separated and then reunited. Significant changes in the Prochlorococcus transcriptome were evident within 6 h of initiating co-culture, with groups of transcripts changing in different temporal waves. Many transcriptional changes persisted throughout the 48 h experiment, suggesting that the presence of the heterotroph affected a stable shift in Prochlorococcus physiology. These initial transcriptome changes largely corresponded to reduced stress conditions for Prochlorococcus, as inferred from the depletion of transcripts encoding DNA repair enzymes and many members of the ‘high light inducible’ family of stress–response proteins. Later, notable changes were seen in transcripts encoding components of the photosynthetic apparatus (particularly, an increase in PSI subunits and chlorophyll synthesis enzymes), ribosomal proteins and biosynthetic enzymes, suggesting that the introduction of the heterotroph may have induced increased production of reduced carbon compounds for export. Changes in secretion-related proteins and transporters also highlight the potential for metabolic exchange between the two strains. 2018-11-14T17:48:32Z 2018-11-14T17:48:32Z 2016-06 Article http://purl.org/eprint/type/JournalArticle 1751-7362 1751-7370 http://hdl.handle.net/1721.1/119005 Biller, Steven J., et al. “Torn Apart and Reunited: Impact of a Heterotroph on the Transcriptome of Prochlorococcus.” The ISME Journal, vol. 10, no. 12, Dec. 2016, pp. 2831–43. https://orcid.org/0000-0002-2638-823X https://orcid.org/0000-0003-1480-2445 en_US http://dx.doi.org/10.1038/ismej.2016.82 The ISME Journal Creative Commons Attribution-Noncommercial-Share Alike http://creativecommons.org/licenses/by-nc-sa/4.0/ application/pdf Nature Publishing Group Prof. Chisholm via Elizabeth Soergel
spellingShingle Biller, Steven
Coe, Allison
Chisholm, Sallie (Penny)
Torn apart and reunited: impact of a heterotroph on the transcriptome of Prochlorococcus
title Torn apart and reunited: impact of a heterotroph on the transcriptome of Prochlorococcus
title_full Torn apart and reunited: impact of a heterotroph on the transcriptome of Prochlorococcus
title_fullStr Torn apart and reunited: impact of a heterotroph on the transcriptome of Prochlorococcus
title_full_unstemmed Torn apart and reunited: impact of a heterotroph on the transcriptome of Prochlorococcus
title_short Torn apart and reunited: impact of a heterotroph on the transcriptome of Prochlorococcus
title_sort torn apart and reunited impact of a heterotroph on the transcriptome of prochlorococcus
url http://hdl.handle.net/1721.1/119005
https://orcid.org/0000-0002-2638-823X
https://orcid.org/0000-0003-1480-2445
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