Genomics Reveals Alga-Associated Cyanobacteria Hiding in Plain Sight COMMENTARY John M

COMMENTARY Genomics reveals alga-associated cyanobacteria hiding in plain sight COMMENTARY John M. Archibalda,b,1 Cyanobacteria occupy a special place in the pantheon of prokaryotic life. It is in the ancestors of these ubiquitous microbes that oxygenic photosynthesis first evolved more than 2 billion y ago (1), and it is from endosymbiotic cyanobacteria that the plastids (chloro- plasts) of plants and algae are derived (2). Modern-day cyanobacteria are diverse in form and function; they include coccoid marine picoplankton such as Prochloro- coccus (3), freshwater biofilm-forming genera [e.g., Gloeomargarita (4)], and filamentous taxa capable of fixing nitrogen [e.g., Nostoc (5)]. In PNAS, Nakayama et al. (6) add an exciting chapter to the story of cyanobacterial diversity. The authors describe the genome sequence of a cyanobacterium living ectosymbiotically on an eye- catching dinoflagellate named Ornithocercus magnificus. Their results provide insight into the nature of an enigmatic symbiotic relationship and reveal the existence of a cryptic, globally distributed cyanobacterial lineage that has until now gone unappreciated. Ornithocercus is indeed magnificent, even by di- Fig. 1. Light micrograph of an Ornithocercus noflagellate standards. The surface of this heterotro- dinoflagellate. The ectosymbiotic OmCyn cyanobacteria phic marine protist is decorated with crown-shaped, are visible within an extracellular chamber on the cellulosic outcroppings that extend from the cell body “upper” crown of the cell. Image courtesy of Takuro Nakayama (Tohoku University, Sendai, Japan). in different directions (Fig. 1) (7). The “upper” crown forms an extracellular chamber in which autofluores- cent cyanobacteria reside, and microscopic evidence genome of the organism, which they dubbed “OmCyn.” suggests that the bacteria can be vertically transmitted In a preliminary phylogenetic analysis of the 16S ribo- from mother to daughter chambers during host cell somal RNA (rRNA) gene, OmCyn was found to branch division (8). First observed more than 100 y ago (9), with members of the Prochlorococcus/Synechococcus the biology of these so-called phaeosomes has long clade. This result was not surprising given the high been mysterious. What type of cyanobacterium are abundance of these well-studied picocyanobacteria— they? How far do they roam? What is the nature of Prochlorococcus is arguably the most abundant organism their interactions with the dinoflagellate host? on Earth (3)—and a previous RT-PCR–based 16S rRNA Nakayama et al. (6) set out to answer these questions survey showed that most dinoflagellate-associated cya- using single-cell genomics. Starting with a solitary O. nobacteria are affiliated with Prochlorococcus/Synecho- magnificus cell plucked from the waters off the port city coccus (10). What was unexpected was the specific of Shimoda, Japan, the cyanobacteria nestled in its evolutionary position of the O. magnificus-associated crown were painstakingly collected with a micropipette cyanobacterium. In search of greater phylogenetic res- and subjected to whole-genome amplification. Using the olution, Nakayama et al. performed a phylogenomic latest short- and long-read DNA sequencing technolo- analysis of 40 proteins, the results of which suggest that gies, the authors succeeded in assembling the entire OmCyn is neither Prochlorococcus nor Synechococcus. aDepartment of Biochemistry & Molecular Biology, Dalhousie University, Halifax, NS, Canada B3H 4R2; and bCentre for Comparative Genomics & Evolutionary Bioinformatics, Dalhousie University, Halifax, NS, Canada B3H 4R2 Author contributions: J.M.A. wrote the paper. The author declares no conflict of interest. Published under the PNAS license. See companion article 10.1073/pnas.1902538116. 1Email: [email protected]. www.pnas.org/cgi/doi/10.1073/pnas.1909788116 PNAS Latest Articles | 1of3 Downloaded by guest on September 30, 2021 The authors conclude that “the OmCyn lineage likely emerged (18). More specifically, Nakayama et al. (6) mapped Tara Oceans soon after the split of the Prochlorococcus lineage and before the short-read sequence data against the OmCyn genome and divergence of Synechococcus subcluster 5.1” (6). against a representative set of 19 picocyanobacterial genomes. The notion that OmCyn is distinct among studied picocyano- As expected, reads mapping to the genomes of the tiny picocyanobacteria was further bolstered by comparative genomics. The bacteria were much more frequently detected in the 0.8- to 5-μm OmCyn genome is ∼1.87 Mbp in size and contains 1,846 protein- organismal size fractions than in larger fractions (i.e., 5 to 20, 20 to coding genes (6). This is a small genome—cyanobacteria with 180, and 180 to 2,000 μm). In stark contrast, 83% of the reads genomes 3 to 5 Mbp in size are common in nature and morpho- mapping to the OmCyn genome were in the 20- to 180-μmsize logically complex species such as Scytonema hofmanni have genomes that are >12 Mbp with >12,000 genes (e.g., ref. 11). In In PNAS, Nakayama et al. add an exciting terms of size and coding capacity, the OmCyn genome is more chapter to the story of cyanobacterial diversity. similar to those of high-light–adapted strains of Prochlorococcus marinus (e.g., MED4) than to the genomes of Synechococcus spp. The authors describe the genome sequence with which it shares more recent common ancestry. In Prochloro- of a cyanobacterium living ectosymbiotically coccus, genome reduction is thought to have occurred as an ad- aptation to life in oligotrophic waters (12, 13), whereas in OmCyn it is on an eye-catching dinoflagellate named presumably a consequence of its ectosymbiotic lifestyle. The OmCyn Ornithocercus magnificus. genome was found to retain only 65% of a set of ∼2,100 core genes/ proteins inferred to have been present in the common ancestor of fraction, precisely where O. magnificus resides [the organism is Synechococcus (subcluster 5.1) and Prochlorococcus (6). Gene fam- 75 to 115 μm in size (19)]. OmCyn sequences were detected in the ilies found to be substantially reduced in OmCyn include those 20- to 180-μm size fractions of samples taken from 51 of 57 Tara involved in “membrane transport” (i.e., communication with its Oceans stations around the world, and the global distribution extracellular environment), and 5 otherwise conserved genes patterns of OmCyn sequences and O. magnificus 18S rDNA se- encoding DNA recombination and repair enzymes have also been quences were found to be highly correlated. Their sequence occur- lost. Although the precise details often vary, gene loss is a recur- rence patterns also correlate with variation in the physicochemical ring theme in bacteria living symbiotically with other organisms, parameters of the water samples such as temperature and iron such as the haptophyte alga-associated cyanobacterium Candidatus concentration. Only 7% of OmCyn-mapping sequences were Atelocyanobacterium thalassa (UCYN-A), the non-photosynthetic, found in the 0.8- to 5-μm fractions analyzed, suggesting that nitrogen-fixing cyanobacteria living within diatoms such as Epithemia the organism rarely, if ever, exists in isolation (such reads could (15), and the cyanobacterium-derived “chromatophores” in the in fact represent cross-fraction contamination due to cell lysis) cytoplasm of the amoeba Paulinella (16). (6). Also, the existence of many OmCyn-like metagenomic reads What does the OmCyn genome reveal about the interplay in the 20- to 180-μm size fractions suggests that a variety of differ- between host and symbiont? Given that O. magnificus is a het- ent Ornithocercus species—not just O. magnificus—harbor cyano- erotroph and OmCyn is a card-carrying phototroph, one obvious bacterial symbionts in nature. possibility is that the latter is providing photosynthate to the Nakayama et al. (6) show that while OmCyn and its kin roam far former. However, OmCyn lives on its host, not within it—it is thus and wide in the world’s oceans they do so in close association with not clear how the exchange of organic carbon would occur. One their dinoflagellate hosts. Their study highlights the power of clue comes from the fact that partially digested OmCyn lookalikes single-cell genomics in exploring the biology of uncultured sym- have been observed in food vacuoles inside Ornithocercus cells biotic microorganisms, and the depth of insight that can be (16). Perhaps OmCyn is a “domesticated breed” of cyanobacteria, obtained when different types of data are cross-referenced. Sym- one that O. magnificus farms on its crown for the purpose of biotic associations between protists and bacteria are extremely supplementing its nutrition (6, 17)! Regardless, what is clear is that common in nature (14–17, 20), and it seems likely that other line- like Synechococcus and Prochlorococcus, the OmCyn genome ages of hitherto overlooked symbiotic bacteria will reveal them- does not encode proteins involved in nitrogen fixation; this is selves as metagenomic datasets continue to grow and we not a factor to consider when pondering the reason(s) for the become better at harnessing the information they contain. The origin and maintenance of this particular symbiotic relationship. results of Nakayama et al. (6) serve to remind us that moving for- Also, while clearly reduced, the OmCyn genome contains enough ward we would do well not to forget the following dictum: Know genes—and the right sorts of genes—to suggest that the thy organism. cyanobacterium is not metabolically dependent on its dinoflagellate host, at least not to any great extent. Acknowledgments Important additional insight into the natural habitat of OmCyn Work in the J.M.A. laboratory is funded by the Natural Sciences and was obtained by analysis of the wealth of metagenomic data Engineering Research Council of Canada and the Gordon and Betty Moore stemming from the recently completed Tara Oceans expedition Foundation. 1 W. W. Fischer, J. Hemp, J. E. Johnson, Evolution of oxygenic photosynthesis. Annu. Rev. Earth Planet. Sci. 44, 647–683 (2016). 2 J. M. Archibald, Endosymbiosis and eukaryotic cell evolution. Curr. Biol. 25, R911–R921 (2015).

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