A Pangenomic Analysis of the Nannochloropsis Organellar Genomes Reveals Novel Genetic Variations in Key Metabolic Genes

Overview

Journal BMC Genomics

Publisher Biomed Central

Specialty Genetics

Date 2014 Mar 21

PMID 24646409

Citations 22

Authors

Shawn R Starkenburg

Kyungyoon J Kwon

Ramesh K Jha

Cedar McKay

Michael Jacobs

Olga Chertkov

Scott Twary

Gabrielle Rocap

Rose Ann Cattolico

Affiliations

Soon will be listed here.

Abstract

Background: Microalgae in the genus Nannochloropsis are photosynthetic marine Eustigmatophytes of significant interest to the bioenergy and aquaculture sectors due to their ability to efficiently accumulate biomass and lipids for utilization in renewable transportation fuels, aquaculture feed, and other useful bioproducts. To better understand the genetic complement that drives the metabolic processes of these organisms, we present the assembly and comparative pangenomic analysis of the chloroplast and mitochondrial genomes from Nannochloropsis salina CCMP1776.

Results: The chloroplast and mitochondrial genomes of N. salina are 98.4% and 97% identical to their counterparts in Nannochloropsis gaditana. Comparison of the Nannochloropsis pangenome to other algae within and outside of the same phyla revealed regions of significant genetic divergence in key genes that encode proteins needed for regulation of branched chain amino synthesis (acetohydroxyacid synthase), carbon fixation (RuBisCO activase), energy conservation (ATP synthase), protein synthesis and homeostasis (Clp protease, ribosome).

Conclusions: Many organellar gene modifications in Nannochloropsis are unique and deviate from conserved orthologs found across the tree of life. Implementation of secondary and tertiary structure prediction was crucial to functionally characterize many proteins and therefore should be implemented in automated annotation pipelines. The exceptional similarity of the N. salina and N. gaditana organellar genomes suggests that N. gaditana be reclassified as a strain of N. salina.

Citing Articles

Toward the Exploitation of Sustainable Green Factory: Biotechnology Use of spp.

Canini D, Ceschi E, Perozeni F Biology (Basel). 2024; 13(5).

PMID: 38785776 PMC: 11117969. DOI: 10.3390/biology13050292.

Identification of Eukaryotic Microalgal Strains.

Fawley M, Fawley K J Appl Phycol. 2021; 32(5):2699-2709.

PMID: 33542589 PMC: 7853647. DOI: 10.1007/s10811-020-02190-5.

Genome sequencing, assembly, and annotation of the self-flocculating microalga Scenedesmus obliquus AS-6-11.

Chen B, Mhuantong W, Ho S, Chang J, Zhao X, Bai F BMC Genomics. 2020; 21(1):743.

PMID: 33109102 PMC: 7590803. DOI: 10.1186/s12864-020-07142-4.

Plastid Genomes and Proteins Illuminate the Evolution of Eustigmatophyte Algae and Their Bacterial Endosymbionts.

Sevcikova T, Yurchenko T, Fawley K, Amaral R, Strnad H, Santos L Genome Biol Evol. 2019; 11(2):362-379.

PMID: 30629162 PMC: 6367104. DOI: 10.1093/gbe/evz004.

Advanced genetic tools enable synthetic biology in the oleaginous microalgae Nannochloropsis sp.

Poliner E, Farre E, Benning C Plant Cell Rep. 2018; 37(10):1383-1399.

PMID: 29511798 DOI: 10.1007/s00299-018-2270-0.

References

von Ballmoos C, Wiedenmann A, Dimroth P . Essentials for ATP synthesis by F1F0 ATP synthases. Annu Rev Biochem. 2009; 78:649-72. DOI: 10.1146/annurev.biochem.78.081307.104803. View

Delcher A, Bratke K, Powers E, Salzberg S . Identifying bacterial genes and endosymbiont DNA with Glimmer. Bioinformatics. 2007; 23(6):673-9. PMC: 2387122. DOI: 10.1093/bioinformatics/btm009. View

Sakihama Y, Nakamura S, Yamasaki H . Nitric oxide production mediated by nitrate reductase in the green alga Chlamydomonas reinhardtii: an alternative NO production pathway in photosynthetic organisms. Plant Cell Physiol. 2002; 43(3):290-7. DOI: 10.1093/pcp/pcf034. View

Carbajo R, Kellas F, Runswick M, Montgomery M, Walker J, Neuhaus D . Structure of the F1-binding domain of the stator of bovine F1Fo-ATPase and how it binds an alpha-subunit. J Mol Biol. 2005; 351(4):824-38. DOI: 10.1016/j.jmb.2005.06.012. View

Barak Z, Chipman D . Allosteric regulation in Acetohydroxyacid Synthases (AHASs)--different structures and kinetic behavior in isozymes in the same organisms. Arch Biochem Biophys. 2011; 519(2):167-74. DOI: 10.1016/j.abb.2011.11.025. View

Quinn J, Yates T, Douglas N, Weyer K, Butler J, Bradley T . Nannochloropsis production metrics in a scalable outdoor photobioreactor for commercial applications. Bioresour Technol. 2012; 117:164-71. DOI: 10.1016/j.biortech.2012.04.073. View

Raman S, Vernon R, Thompson J, Tyka M, Sadreyev R, Pei J . Structure prediction for CASP8 with all-atom refinement using Rosetta. Proteins. 2009; 77 Suppl 9:89-99. PMC: 3688471. DOI: 10.1002/prot.22540. View

Le Corguille G, Pearson G, Valente M, Viegas C, Gschloessl B, Corre E . Plastid genomes of two brown algae, Ectocarpus siliculosus and Fucus vesiculosus: further insights on the evolution of red-algal derived plastids. BMC Evol Biol. 2009; 9:253. PMC: 2765969. DOI: 10.1186/1471-2148-9-253. View

Regalia M, Alm Rosenblad M, Samuelsson T . Prediction of signal recognition particle RNA genes. Nucleic Acids Res. 2002; 30(15):3368-77. PMC: 137091. DOI: 10.1093/nar/gkf468. View

10.

Kim D, Chivian D, Baker D . Protein structure prediction and analysis using the Robetta server. Nucleic Acids Res. 2004; 32(Web Server issue):W526-31. PMC: 441606. DOI: 10.1093/nar/gkh468. View

11.

LARKIN M, Blackshields G, Brown N, Chenna R, McGettigan P, McWilliam H . Clustal W and Clustal X version 2.0. Bioinformatics. 2007; 23(21):2947-8. DOI: 10.1093/bioinformatics/btm404. View

12.

Pan K, Qin J, Li S, Dai W, Zhu B, Jin Y . NUCLEAR MONOPLOIDY AND ASEXUAL PROPAGATION OF NANNOCHLOROPSIS OCEANICA (EUSTIGMATOPHYCEAE) AS REVEALED BY ITS GENOME SEQUENCE(1). J Phycol. 2016; 47(6):1425-32. DOI: 10.1111/j.1529-8817.2011.01057.x. View

13.

Hollingshead S, Kopecna J, Jackson P, Canniffe D, Davison P, Dickman M . Conserved chloroplast open-reading frame ycf54 is required for activity of the magnesium protoporphyrin monomethylester oxidative cyclase in Synechocystis PCC 6803. J Biol Chem. 2012; 287(33):27823-33. PMC: 3431679. DOI: 10.1074/jbc.M112.352526. View

14.

Finn R, Mistry J, Tate J, Coggill P, Heger A, Pollington J . The Pfam protein families database. Nucleic Acids Res. 2009; 38(Database issue):D211-22. PMC: 2808889. DOI: 10.1093/nar/gkp985. View

15.

Bennett S . Solexa Ltd. Pharmacogenomics. 2004; 5(4):433-8. DOI: 10.1517/14622416.5.4.433. View

16.

Wei L, Xin Y, Wang D, Jing X, Zhou Q, Su X . Nannochloropsis plastid and mitochondrial phylogenomes reveal organelle diversification mechanism and intragenus phylotyping strategy in microalgae. BMC Genomics. 2013; 14:534. PMC: 3750441. DOI: 10.1186/1471-2164-14-534. View

17.

Jones D . Protein secondary structure prediction based on position-specific scoring matrices. J Mol Biol. 1999; 292(2):195-202. DOI: 10.1006/jmbi.1999.3091. View

18.

Vieler A, Wu G, Tsai C, Bullard B, Cornish A, Harvey C . Genome, functional gene annotation, and nuclear transformation of the heterokont oleaginous alga Nannochloropsis oceanica CCMP1779. PLoS Genet. 2012; 8(11):e1003064. PMC: 3499364. DOI: 10.1371/journal.pgen.1003064. View

19.

Andersen R, Brett R, Potter D, Sexton J . Phylogeny of the Eustigmatophyceae Based upon 18S rDNA, with Emphasis on Nannochloropsis. Protist. 2012; 149(1):61-74. DOI: 10.1016/S1434-4610(98)70010-0. View

20.

Weibezahn J, Schlieker C, Bukau B, Mogk A . Characterization of a trap mutant of the AAA+ chaperone ClpB. J Biol Chem. 2003; 278(35):32608-17. DOI: 10.1074/jbc.M303653200. View