Novel metabolism in Chlamydomonas through the lens of genomics

Chlamydomonas has traditionally been exploited as an organism that is associated with sophisticated physiological, genetic and molecular analyses, all of which have been used to elucidate several biological processes, especially photosynthesis and flagella function and assembly. Recently, the genomics of Chlamydomonas has been combined with other technologies to unveil new aspects of metabolism, including inorganic carbon utilization, anaerobic fermentation, the suite and functions of selenoproteins, and the regulation of vitamin biosynthesis. These initial findings represent the first glimpse through a genomic window onto the highly complex metabolisms that characterize a unicellular, photosynthetic eukaryote that has maintained both plant-like and animal-like characteristics over evolutionary time.

Introduction

Chlamydomonas reinhardtii is a member of the green algal lineage that diverged from the streptophytes approximately one billion years ago. It has served as an outstanding model organism, especially for analyzing eukaryotic chloroplast biology and the biogenesis and action of flagella and basal bodies [1, 2, 3]. Genetic analyses with this organism began in the mid 20th century and developed into sophisticated molecular and genomic technologies for dissecting biological processes. Unique attributes that make Chlamydomonas ideal for dissecting photosynthesis are its ability to grow heterotrophically in the dark by metabolizing exogenous acetate, and its maintenance of a normal green chloroplast that retains the capacity to perform oxygenic photosynthesis when illuminated following growth in the dark. These characteristics have allowed the isolation of a range of mutants in which the function and biogenesis of the photosynthetic apparatus is adversely affected [1, 4]. Most other photosynthetic organisms and all vascular plants either do not survive or exhibit growth retardation and pigment loss in the absence of photosynthesis. Recent work on photosynthesis in Chlamydomonas has focused on the discovery of molecules that catalyze the assembly of the photosynthetic apparatus and determine the abundance and rate of synthesis of individual complexes, and regulatory molecules that control the distribution of excitation energy (state transitions) or dissipation of excess absorbed light energy (non-photochemical quenching) [2, 5, 6].

Many molecular technologies have also been applied to studies of Chlamydomonas. The chloroplast and nuclear genomes of this alga are readily transformed [7]. Plasmid, cosmid, and bacterial artificial chromosome (BAC) libraries are available. Methods have been developed to generate and identify tagged mutant alleles. Alleles that are not tagged can be identified by map-based cloning [8, 9••]. Gene function can be evaluated by suppression of specific gene activities using antisense or RNA interference (RNAi) constructs [10], and reporter genes have been developed to identify regulatory factors and sequences that are involved in regulating gene expression [11].

In this review, we discuss how the genomics of Chlamydomonas are being combined with these other technologies to unveil new aspects of metabolism, including inorganic carbon utilization, anaerobic fermentation, the suite and functions of selenoproteins, and the regulation of vitamin biosynthesis. The facts and concepts discussed below represent initial insights into the highly complex metabolisms that characterize a unicellular, photosynthetic eukaryote.