COMMENTARY

Genome complexity in a lean, mean photosynthetic machine

John M. Archibald* Canadian Institute for Advanced Research, Program in Evolutionary Biology, and Department of Biochemistry and Molecular Biology, Dalhousie University, Sir Charles Tupper Medical Building, 5850 College Street, Halifax, NS, Canada B3H 1X5

hotosynthetic organisms come in et al. (1) weighs in at 12.56 Mbp, mak- all shapes and sizes. From a hu- ing it among the smallest, although not man perspective, the trees and the smallest, nuclear of a free- plants of dry land are the most living characterized thus far Pconspicuous examples, but the next time [that honor belongs to the 9.2-Mbp ge- you admire a colorful tulip or marvel at nome of the fungus Ashbya gossypii the girth of a giant Sequoia, consider (14)]. The O. tauri genome is composed the following: Approximately half of the of 20 linear chromosomes between 1.07 oxygen we breathe is generated by single- and 0.16 Mbp (1) and, given its small celled photosynthesizers, phytoplankton, size, is remarkable in the number of adrift in the world’s , invisible to genes it encodes: 8,166 protein-coding the naked eye and unfathomably large genes are predicted (6,265 by similarity in number, quietly harnessing solar en- to known genes), far more than in the ergy, fixing carbon dioxide, and produc- Ϸ16-Mbp genome of the red alga Cyan- ing oxygen by the bucket-load. In this idioschyzon merolae (5,331 genes) (15) issue of PNAS, Derelle et al. (1) present or in the Ϸ12-Mbp genome of the labo- the complete genome sequence of the ratory yeast Saccharomyces cerevisiae smallest of the small eukaryotic (nucle- (6,563 genes) (16). With a mean inter- us-containing) phytoplankton, Ostreo- genic distance of only 197 bp, an aver- coccus tauri. This organism is best Fig. 1. Transmission electron micrograph of O. age intron size of 103 bp, and multiple known for its diminutive cell size, about tauri strain OTH95, modified and reproduced gene fusions, the O. tauri genome ap- that of a typical bacterium. Its genome with permission from Herve´Moreau (Universite´ pears to be the product of intense ge- is equally remarkable for its small size Paris, Paris, France). C, ; S, starch gran- nome compaction. One wonders to what ule; M, ; N, nucleus. and extreme compactness. However, the extent the complexities of transcription O. tauri genome is also unexpectedly initiation and termination have been complex and provides a fascinating refs. 6–8). O. tauri was first discovered affected. glimpse into the genetic makeup and in 1994 in France’s Thau lagoon, a shal- In terms of structure, the most un- metabolic potential of the smallest low offshoot of the Mediterranean Sea usual feature of the O. tauri genome is known eukaryote at the base of the ma- known for its oyster farming. Barely 1 its heterogeneity. The genome as a rine food chain. ␮m in diameter and practically invisible whole has a GϩC content of Ϸ58%, but Oxygenic photosynthesis first evolved under the light microscope, O. tauri was chromosome 19 and approximately half in the ancestors of modern-day cya- detected by flow cytometry and hailed of chromosome 2 differ significantly nobacteria. In terms of sheer numbers, as the ‘‘smallest eukaryotic organism’’ from this average (54% and 52% GϩC, these organisms dominate the (2), (9). It also proved to be shockingly sim- respectively) and contain 77% of the but from the perspective of primary pro- ple in its ultrastructure: O. tauri cells 417 transposable elements encoded in ductivity, eukaryotic algae are consid- lack flagella and a and contain the genome (1). Genes encoded in the ered more significant. Marine diatoms, one mitochondrion, one chloroplast, a low GϩC portion of chromosome 2 also for example, produce up to 40% of the single , and a nucleus exhibit a different codon usage pattern organic carbon generated in the ocean containing a single nuclear pore (Fig. 1) than genes elsewhere in the genome, each year (3) and represent just one of (10). Molecular data (11, 12) indicate and they possess smaller and more com- the abundant and well studied algal lin- that O. tauri belongs to a group of positionally biased introns. From a phy- eages in the sea. Least understood of all called prasinophytes, a lin- logenetic perspective, 43% of the genes eukaryotic phytoplankton are those with eage thought to be of key importance on chromosome 2 are most similar to a diameter of Ͻ2–3 ␮m, the so-called in elucidating the earliest events in the green algal homologs, which is a similar ‘‘picoeukaryotes.’’ The first descriptions evolution of chlorophyll b-containing proportion to that seen for the other of bacterial-sized date back organisms. O. tauri appears to be ubiq- chromosomes (excluding chromosome more than 40 years (e.g., ref. 4), but it is uitous in coastal waters and in the open 19). Therefore, despite its anomalous only with the application of flow cytom- ocean (e.g., refs. 6, 8, and 12), and its composition and structure, there is no etry (2) and molecular approaches (5) minimal cell structure and high growth evidence that the low GϩC region of to the study of marine microbes that we rate have made it a promising model chromosome 2 is of exogenous origin. have begun to grasp the extent of their picoeukaryote. Derelle et al. (1) raise the possibility abundance and diversity. Preliminary molecular investigations that it is a sex chromosome, citing the O. tauri is perhaps the most famous of pegged the O. tauri genome at well un- all picoeukaryotes and, together with its der 15 megabase pairs (Mbp) (11), and, close relatives, has become the focus of like most model organisms these days, Conflict of interest statement: No conflicts declared. concerted efforts to understand the O. tauri quickly became the focus of a See companion article on page 11647. global distribution and ecological signifi- genome project (13). The complete ge- *E-mail: [email protected]. cance of eukaryotic picoplankton (e.g., nome sequence presented by Derelle © 2006 by The National Academy of Sciences of the USA

www.pnas.org͞cgi͞doi͞10.1073͞pnas.0605255103 PNAS ͉ August 1, 2006 ͉ vol. 103 ͉ no. 31 ͉ 11433–11434 Downloaded by guest on September 25, 2021 fact that bona fide sex chromosomes in present, as is a complex gene family those in Chlamydomonas (1). If C4 pho- other organisms are often similarly rid- encoding prasinophyte-specific light- tosynthesis does exist, it is not difficult dled with transposable elements (17). harvesting antenna proteins. Most to imagine the competitive advantage it Meiosis has never been observed in O. unexpected is the presence of genes would bestow on O. tauri cells under tauri, although the presence of a near- implicated in C4 photosynthesis. This conditions of high cell density and low complete set of meiotic genes encoded process has evolved repeatedly in CO2 levels. in its genome (1) suggests that sex is at higher plants as an adaptation to envi- In summary, given its small size, the least a possibility. ronmental stress (e.g., drought and low O. tauri genome packs plenty of sur- The composition of chromosome 19 is CO2 concentrations) and involves mod- prises. However, as is so often the case even more intriguing. More than 60% of ifications to leaf structure and altered in , the biological the predicted protein genes on this chro- biochemistry (reviewed in ref. 18). The significance of many of its interesting mosome have no similarity to known existence of bona fide C4 photosynthe- features will be fully revealed only by genes, and, of those that do, only 18% sis in phytoplankton is controversial. comparison to closely related . are demonstrably green algal in origin. The morphological transformations It is therefore significant that the strain The bulk of the remaining genes appear that occur in plants are obviously im- sequenced by Derelle et al. (1) (OTH95, most similar to bacterial homologs (al- possible for a microbe, but an intracel- the original Thau Lagoon isolate) is the though modestly so), and a significant lular C4 cycle has been documented first of a trio of complete fraction of the non-green algal genes are genomes soon to be available. The Joint predicted to encode surface membrane Genome Institute (www.jgi.doe.gov) has proteins and proteins involved in glyco- The most already sequenced the genome of a Cali- conjugate synthesis (1). Based on these fornian surface-isolated strain (CCE9901; observations, the authors hypothesize unusual feature of see ref. 8) and is now sequencing a ‘‘low- that chromosome 19 has a different evo- light’’ strain from the Atlantic Ocean lutionary history than the rest of the the Ostreococcus tauri (RCC141; see ref. 7). Recent work by genome (1). Given that O. tauri lacks a Moreau, Vaulot, and colleagues (7) has cell wall and is susceptible to grazing in genome is its revealed that these and other Ostreococcus nature (8), it is tempting to speculate strains constitute different ‘‘ecotypes’’ that the cell surface genes on chromo- heterogeneity. with distinct growth patterns, karyo- some 19 were acquired by lateral gene types, and pigment compositions. As transfer and selected for as an adapta- was the case for the cyanobacterium tion to predation. If this is true, how- in several plants, including the aquatic Prochlorococcus (20), a comparison of ever, how these genes were acquired, monocot Hydrilla verticillata (19). O. the genomic differences between ecolog- and from where, remains a mystery. tauri appears to possess the right com- ically distinct Ostreococcus strains should What does the O. tauri genome reveal bination of enzymes in the right cellu- greatly improve our understanding of about the cell biology and metabolism lar locations to drive such a process, the genetic determinants of niche adap- of this tiny organism? The genome pos- including a putatively cytosolic phos- tation in oceanic picoplankton commu- sesses complete or nearly complete gene phoenolpyruvate carboxylase and at nities. Despite its size, the ease with sets for proteins involved in cell divi- least one chloroplast-targeted NADP- which Ostreococcus (and other prasino- sion, starch metabolism, and nitrogen dependent malic enzyme. Much experi- phytes) can be cultured and studied in assimilation, as well as a diverse set of mentation will be required to determine the laboratory makes it a promising transcription factors and proteins with whether C4 photosynthesis actually oc- target for even more ambitious attempts putative kinase- and calcium-binding curs in the tiny cells of O. tauri, but it is to study the diversity and evolution of domains (1). As expected, a complete significant that its genome does not en- eukaryotic picoplankton using the com- suite of enzymes essential for carbon code any obvious ‘‘carbon-concentrating bined strengths of oceanography, micro- fixation and the Calvin cycle are mechanism’’ genes comparable with bial ecology, and comparative genomics.

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