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Selection-Enriched Genomic Loci (SEGL) Reveals Genetic Loci for Environmental Adaptation and Photosynthetic Productivity in Chlamydomonas reinhardtii

View ORCID ProfileBen F. Lucker, View ORCID ProfileNicolas L. Panchy, Joshua A. Temple, Urs F. Benning, Jacob D. Bibik, Peter G. Neofotis, Joseph C. Weissman, View ORCID ProfileIvan R. Baxter, View ORCID ProfileShin-Han Shiu, View ORCID ProfileDavid M. Kramer
doi: https://doi.org/10.1101/2021.07.06.451237
Ben F. Lucker
1DOE-Plant Research Laboratory, Michigan State University, East Lansing, MI 48824-1312, USA
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  • For correspondence: benflucker@gmail.com
Nicolas L. Panchy
2Genetics Graduate Program, Michigan State University, East Lansing, MI 48824-1312, USA
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Joshua A. Temple
1DOE-Plant Research Laboratory, Michigan State University, East Lansing, MI 48824-1312, USA
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Urs F. Benning
1DOE-Plant Research Laboratory, Michigan State University, East Lansing, MI 48824-1312, USA
3Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, MI 48824-1312, USA
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Jacob D. Bibik
1DOE-Plant Research Laboratory, Michigan State University, East Lansing, MI 48824-1312, USA
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Peter G. Neofotis
1DOE-Plant Research Laboratory, Michigan State University, East Lansing, MI 48824-1312, USA
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Joseph C. Weissman
6Corporate Strategic Research, ExxonMobil, Annandale, NJ 08801
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Ivan R. Baxter
7Donald Danforth Plant Science Center, St. Louis, MO 63132
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Shin-Han Shiu
2Genetics Graduate Program, Michigan State University, East Lansing, MI 48824-1312, USA
4Department of Plant Biology, Michigan State University, East Lansing, MI 48824-1312, USA
5Department Computational Mathematics, Science, and Engineering, Michigan State University, East Lansing, MI 48824-1312, USA
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David M. Kramer
1DOE-Plant Research Laboratory, Michigan State University, East Lansing, MI 48824-1312, USA
3Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, MI 48824-1312, USA
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  • For correspondence: benflucker@gmail.com
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Abstract

This work demonstrates an approach to produce and select hybrid algal strains exhibiting increased photosynthetic productivity under multiple environmental conditions. This simultaneously addresses two major impediments to improving algal bioenergy production: 1) generating new genetic variants with improved performance; and 2) disentangling complex interactions between genetic and physiological factors contributing to these improvements. We pooled progeny generated from mating two environmental isolates of the green alga Chlamydomonas reinhardtii and cultured the pools under multiple environmental conditions. Strains from the outcompeting populations showed substantial (in some cases over 3 fold) increases in productivity over the parental lines under certain environments related to biomass production, including laboratory conditions as well as hyperoxia, fluctuating light, high salinity and high temperature. The results indicate that C. reinhardtii has remarkable, untapped, directed evolution capacity that may be harnessed using breeding and competition approaches. The populations were deep sequenced at multiple time points to identify “Selection-Enriched Genomic Loci” (SEGL) that accumulated in the populations, and thus likely confer increased fitness under the respective environmental conditions. With improved resolution, SEGL mapping can identify allelic combinations used for targeted breeding approaches, generating elite algal lines with multiple desirable traits, as well as to further understand the genetic and mechanistic bases of photosynthetic productivity.

Significance Statement Increasing the photosynthetic efficiency of algae during biomass production is perhaps the most critical hurdle for economically sustainable algal based biofuels. This presents unique challenges because modifications designed to increase photosynthesis often result in decreased fitness, due to production of toxic reactive oxygen species when photosynthesis is not adequately regulated. These problems are exacerbated under natural and outdoor production environments because of the complex nature of photosynthesis and the multifaceted interactions between genetic, environmental and physiological factors. Here, we demonstrate a high throughput biotechnological screening approach that simultaneously produces algal strains with highly increased autotrophic productivity and identifies genomic loci contributing to these improvements. Our results demonstrate that Chlamydomonas reinhardtii exhibits high directed evolutionary capacity readily accessed through breeding and selection.

Competing Interest Statement

The work was supported in part by the ExxonMobil Corporation and took advantage of experimental platform developed in the Kramer lab at MSU and has been licensed to Phenometrics, Inc. (www.phenometricsinc.com), of which Lucker and Kramer own shares.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted July 06, 2021.
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Selection-Enriched Genomic Loci (SEGL) Reveals Genetic Loci for Environmental Adaptation and Photosynthetic Productivity in Chlamydomonas reinhardtii
Ben F. Lucker, Nicolas L. Panchy, Joshua A. Temple, Urs F. Benning, Jacob D. Bibik, Peter G. Neofotis, Joseph C. Weissman, Ivan R. Baxter, Shin-Han Shiu, David M. Kramer
bioRxiv 2021.07.06.451237; doi: https://doi.org/10.1101/2021.07.06.451237
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Selection-Enriched Genomic Loci (SEGL) Reveals Genetic Loci for Environmental Adaptation and Photosynthetic Productivity in Chlamydomonas reinhardtii
Ben F. Lucker, Nicolas L. Panchy, Joshua A. Temple, Urs F. Benning, Jacob D. Bibik, Peter G. Neofotis, Joseph C. Weissman, Ivan R. Baxter, Shin-Han Shiu, David M. Kramer
bioRxiv 2021.07.06.451237; doi: https://doi.org/10.1101/2021.07.06.451237

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