The Mixed Lineage Nature of Nitrogen Transport and Assimilation in Marine Eukaryotic Phytoplankton: A Case Study of Micromonas

McDonald, Sarah M.; Plant, Joshua N.; Worden, Alexandra Z.

doi:10.1093/molbev/msq113

Title: The Mixed Lineage Nature of Nitrogen Transport and Assimilation in Marine Eukaryotic Phytoplankton: A Case Study of Micromonas

Journal Article · Sun May 09 00:00:00 EDT 2010 · Molecular Biology and Evolution

DOI:https://doi.org/10.1093/molbev/msq113· OSTI ID:1625396

McDonald, Sarah M. ^[1]; Plant, Joshua N. ^[1]; Worden, Alexandra Z. ^[1]

Monterey Bay Aquarium Research Inst., Moss Landing, CA (United States)

The prasinophyte order Mamiellales contains several widespread marine picophytoplankton (≤ 2 lm diameter) taxa, including Micromonas and Ostreococcus. Complete genome sequences are available for two Micromonasisolates, CCMP1545 and RCC299. We performed in silico analyses of nitrogen transporters and related assimilation genes in CCMP1545 and RCC299 and compared these with other green lineage organisms as well as Chromalveolata, fungi, bacteria, and archaea. Phylogenetic reconstructions of ammonium transporter (AMT) genes revealed divergent types contained within each Mamiellales genome. Some were affiliated with plant and green algal AMT1 genes and others with bacterial AMT2 genes. Land plant AMT2 genes were phylogenetically closer to archaeal transporters than to Mamiellales AMT2 genes. The Mamiellales represent the first green algal genomes to harbor AMT2 genes, which are not found in Chlorella and Chlamydomonas or the chromalveolate algae analyzed but are present in oomycetes. Fewer nitrate transporter (NRT) than AMT genes were identified in the Mamiellales. NRT1 was found in all but CCMP1545 and showed highest similarity to Mamiellales and proteobacterial NRTs. NRT2 genes formed a bootstrap-supported clade basal to other green lineage organisms. Several nitrogen-related genes were colocated, forming a nitrogen gene cluster. Overall, RCC299 showed the most divergent suite of nitrogen transporters within the various Mamiellales genomes, and we developed TaqMan quantitative polymerase chain reaction primer–probes targeting a subset of these, as well as housekeeping genes, in RCC299. All those investigated showed expression either under standard growth conditions or under nitrogen depletion. Like other recent publications, our findings show a higher degree of ‘‘mixed lineage gene affiliations’’ among eukaryotes than anticipated, and even the most phylogenetically anomalous versions appear to be functional. Nitrogen is often considered a regulating factor for phytoplankton populations. This study provides a springboard for exploring the use and functional diversification of inorganic nitrogen transporters and related genes in eukaryotic phytoplankton.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division; National Science Foundation (NSF); Gordon and Betty Moore Foundation

Grant/Contract Number:: AC02-05CH11231; OCE-0623928; OCE-0836721

OSTI ID:: 1625396

Journal Information:: Molecular Biology and Evolution, Vol. 27, Issue 10; ISSN 0737-4038

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United States

Language:: English

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Contrasting Mixotrophic Lifestyles Reveal Different Ecological Niches in Two Closely Related Marine Protists Wilken, Susanne; Choi, Chang Jae; Worden, Alexandra Z. Journal of Phycology, Vol. 56, Issue 1 https://doi.org/10.1111/jpy.12920	journal	November 2019
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Targeted metagenomic recovery of four divergent viruses reveals shared and distinctive characteristics of giant viruses of marine eukaryotes Needham, David M.; Poirier, Camille; Hehenberger, Elisabeth Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 374, Issue 1786 https://doi.org/10.1098/rstb.2019.0086	journal	October 2019
Evolutionary classification of ammonium, nitrate, and peptide transporters in land plants von Wittgenstein, Neil JJB; Le, Cuong H.; Hawkins, Barbara J. BMC Evolutionary Biology, Vol. 14, Issue 1 https://doi.org/10.1186/1471-2148-14-11	journal	January 2014
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Algal MIPs, high diversity and conserved motifs Anderberg, Hanna I.; Danielson, Jonas ÅH; Johanson, Urban BMC Evolutionary Biology, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2148-11-110	journal	April 2011
Retained duplicate genes in green alga Chlamydomonas reinhardtii tend to be stress responsive and experience frequent response gains Wu, Guangxi; Hufnagel, David E.; Denton, Alisandra K. BMC Genomics, Vol. 16, Issue 1 https://doi.org/10.1186/s12864-015-1335-5	journal	January 2015
Growth on ATP Elicits a P-Stress Response in the Picoeukaryote Micromonas pusilla Whitney, LeAnn P.; Lomas, Michael W. PLOS ONE, Vol. 11, Issue 5 https://doi.org/10.1371/journal.pone.0155158	journal	May 2016
Responses of the picoprasinophyte Micromonas commoda to light and ultraviolet stress Cuvelier, Marie L.; Guo, Jian; Ortiz, Alejandra C. PLOS ONE, Vol. 12, Issue 3 https://doi.org/10.1371/journal.pone.0172135	journal	March 2017
Utilization of urea and expression profiles of related genes in the dinoflagellate Prorocentrum donghaiense Jing, Xiaoli; Lin, Senjie; Zhang, Huan PLOS ONE, Vol. 12, Issue 11 https://doi.org/10.1371/journal.pone.0187837	journal	November 2017
Identifying reference genes with stable expression from high throughput sequence data Alexander, Harriet; Jenkins, Bethany D.; Rynearson, Tatiana A. Frontiers in Microbiology, Vol. 3 https://doi.org/10.3389/fmicb.2012.00385	journal	January 2012
Conserved Transcriptional Responses to Nutrient Stress in Bloom-Forming Algae Harke, Matthew J.; Juhl, Andrew R.; Haley, Sheean T. Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.01279	journal	July 2017
Sequence and expression analysis of the AMT gene family in poplar Wu, Xiangyu; Yang, Han; Qu, Chunpu Frontiers in Plant Science, Vol. 6 https://doi.org/10.3389/fpls.2015.00337	journal	May 2015

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59 BASIC BIOLOGICAL SCIENCES
54 ENVIRONMENTAL SCIENCES
biochemistry & molecular biology
evolutionary biology
genetics & heredity
nitrogen
Micromonas
Ostreococcus
green algae
green lineage
quantitative PCR
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phylogeny

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