4.8 Article

Genomic Analysis of Picochlorum Species Reveals How Microalgae May Adapt to Variable Environments

Journal

MOLECULAR BIOLOGY AND EVOLUTION
Volume 35, Issue 11, Pages 2702-2711

Publisher

OXFORD UNIV PRESS
DOI: 10.1093/molbev/msy167

Keywords

environmental adaptation; genome reduction; horizontal gene transfer; green algae; biallelic divergence

Funding

  1. Department of Energy [DE-EE0003373/001]
  2. National Science Foundation Integrative Graduate Education and Research Traineeship for Renewable and Sustainable fuels program at Rutgers University [0903675]
  3. Phycological Society of America
  4. Collaborative Genome Program of the Korea Institute of Marine Science and Technology Promotion (KIMST) - Ministry of Oceans and Fisheries (MOF) [20180430]
  5. National Research Foundation of Korea [NRF-2017R1A2B3001923]
  6. Next-generation BioGreen21 Program from the Rural Development Administration, Korea [PJ011121]
  7. Rutgers University School of Environmental and Biological Sciences Genome Cooperative
  8. Division Of Graduate Education
  9. Direct For Education and Human Resources [0903675] Funding Source: National Science Foundation

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Understanding how microalgae adapt to rapidly changing environments is not only important to science but can help clarify the potential impact of climate change on the biology of primary producers. We sequenced and analyzed the nuclear genome of multiple Picochlorum isolates (Chlorophyta) to elucidate strategies of environmental adaptation. It was previously found that coordinated gene regulation is involved in adaptation to salinity stress, and here we show that gene gain and loss also play key roles in adaptation. We determined the extent of horizontal gene transfer (HGT) from prokaryotes and their role in the origin of novel functions in the Picochtorum Glade. HGT is an ongoing and dynamic process in this algal Glade with adaptation being driven by transfer, divergence, and loss. One HGT candidate that is differentially expressed under salinity stress is indolepyruvate decarboxylase that is involved in the production of a plant auxin that mediates bacteria-diatom symbiotic interactions. Large differences in levels of heterozygosity were found in diploid haplotypes among Picochlorum isolates. Biallelic divergence was pronounced in P. oldahomensis (salt plains environment) when compared with its closely related sister taxon Picochlorum SENEW3 (brackish water environment), suggesting a role of diverged alleles in response to environmental stress. Our results elucidate how microbial eukaryotes with limited gene inventories expand habitat range from mesophilic to halophilic through allelic diversity, and with minor but important contributions made by HGT. We also explore how the nature and quality of genome data may impact inference of nuclear ploidy.

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