Current Biology Magazine Quick guide Prochlorococcus Sallie W. Chisholm What is Prochlorococcus? Take a syringe of seawater from almost anywhere in ...

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Current Biology

Magazine Quick guide

Prochlorococcus Sallie W. Chisholm What is Prochlorococcus? Take a syringe of seawater from almost anywhere in tropical or sub-tropical oceans and inject it into a flow cytometer. As the indigenous microbes pass through the focused laser beam, they will scatter light according to their size, and autofluoresce according to their pigments. The smallest cells that emit red chlorophyll fluorescence are Prochlorococcus (Figure 1), and this is precisely how they were discovered 30 years ago. We now know that there are 100 million of these tiny powerhouses in each liter of seawater over vast ocean regions. Good heavens! How could we have missed seeing them before? Less than a micron in diameter, they could barely be seen with the light or epifluorescence microscopes available at the time. If visible at all, they were thought to be chloroplasts from lysed eukaryotic cells. Although, in hindsight, there were hints as to their existence, their vast distribution and incredible abundance was only appreciated with the advent of sea-going flow cytometry. OK, OK, but what IS it? And why is it called Prochlorococcus? Prochlorococcus is a cyanobacterium — a bacterium that does oxygenic photosynthesis — and its name is actually a historical misnomer. Prochlorococcus contains chlorophyll b, rather than the phycobilisomes that are typical of most other cyanobacteria. At the time of its discovery, the only other chlorophyllb-containing cyanobacteria were Prochloron (an invertebrate symbiont) and Prochlorothrix (a freshwater chain former). Because chlorphyll b is a characteristic of eukaryotic green algae (members of the Chlorophyta), they were called ‘prochlorophytes’. Lacking any other characteristic phenotype, this new coccoid member of the prokaryotic chlorophyll-b club was called Prochlorococcus. Molecular phylogenies soon shattered this grouping by revealing that

Prochlorococcus is simply a smaller, differently pigmented variant of marine Synechococcus, which had been discovered a decade earlier. Prochlorococcus is not closely related to the other prochlorophytes, and it appears that the chlorophyll-b trait evolved independently in each of them — as it did in the ancestor of eukaryotic cell chloroplasts. OK, so what’s so special about Prochlorococcus? Why all the fuss? It’s the smallest and most abundant photosynthetic cell on Earth. There are an estimated 3 x 1027 of them in the global oceans, collectively weighing twice as much as all humans, and sporting a surface area 100 times that of the Earth. They constitute half of the chlorophyll over vast ocean ecosystems, single-handedly supplying significant amounts of organic carbon to the rest of the microbial food web. About the size of the wavelengths of light they absorb, they are extremely efficient photosynthetic machines, and their genomes represent one of the most streamlined blueprints for life. With a lower bound of 1,800 genes, they synthesize biomass using only solar energy, CO2 and inorganic compounds. That’s minimal life. That’s impressive! Wait a minute… How can they be a single species and dominate the ecosystem? That violates basic ecological theory. Indeed, all Prochlorococcus belong to the same ‘species’, if one uses the classical bacterial taxonomy yardstick of less than 3% divergence in 16S rRNA sequence. But underlying Prochlorococcus’ sheer abundance and global population stability is an extraordinary amount of genomic diversity, in terms of both genome size and gene content. Each cell has between 1,800 and 2,700 genes, only about 1,000 of which — their core — are shared by all lineages. The balance are flexible genes — some shared with a subset of other lineages, and some unique to one in particular. These genes are drawn, over millions of years, from the massive reservoir of microbial genes, and define the nano-niche of each Prochlorococcus lineage. Evidence suggests that there are hundreds of ecologically

Figure 1. Prochlorococcus — a messenger from the sea. Prochlorococcus cells as they appear under an epifluorescence microscope when excited by blue light. The red fluorescence is from their chlorophyll. Each cell is about 0.6 m in diameter. Photo by J. Berta-Thompson.

distinct Prochlorococcus populations in each milliliter of seawater and we have just begun to appreciate the extent of its diversity. With each new genome sequenced, 100–200 entirely new genes are discovered. Indeed, the global collective genome (the pangenome) of Prochlorococcus is estimated to be about 80,000 genes — four times the size of the human genome. What’s it like to be a Prochlorococcus cell? Life is simple and your world is dilute! Although you are surrounded by other Prochlorococcus cells, they are 100 body lengths away, and the atoms of trace metals you must acquire are 2–4 body lengths away. As the sun comes up you photosynthesize and grow. By late afternoon you begin to replicate your chromosome, and as night falls you are ready to divide into two daughter cells. You passively drift away from your sister and are tens of meters away within an hour and kilometers away within a week. Odds are that one of you will die within two days of being born, likely through phage infection or becoming a meal for a small protist. Thus, day in and day out the total number of Prochlorococcus cells stays roughly

Current Biology 27, R431–R510, June 5, 2017 © 2017 Elsevier Ltd. R447

Current Biology

Magazine the same, because reproduction balances the losses. What other roles do phage play? We have begun to view phage that lyse Prochlorococcus not so much as predators, but as an integral part of the overall system. Even though they kill the cell they infect, that cell has a plethora of identical clones drifting throughout the ocean; its demise is not going to destroy the lineage. Furthermore, phage appear to help maintain diversity through their so-called ‘kill-the-winner’ infection dynamics. Finally, many of the phage that infect Prochlorococcus carry genes with homology to host metabolic genes — for example, those related to phosphorus acquisition or even photosynthesis — that they use to redirect host metabolism to their own ends. It appears that these genes can be swapped in and out of host genomes, evolving under different selective pressures whilst in the phage. Thus, phage can be an incubator for generating gene diversity and a shuttle service for moving genes around. You call Prochlorococcus a ‘messenger’. What’s that all about? Patterns of diversity in Prochlorococcus emerge from the selective pressures in different habitats. Decoding those patterns and relating them to environmental variables help us discover the strongest selective agents. This became obvious early on with the discovery of high and low light-adapted ecotypes, whose fitness is dramatically different at different light intensities; a light level that is lethal for one strain can be near optimal for another. Furthermore, different lineages carry different phosphorus and iron-acquisition genes, depending on their ocean of origin. Sometimes the patterns are not obvious, but the search itself guides us toward interesting areas to explore. Take nitrogen, for example. The availability of nitrogen is an important limiting factor in the oceans; add nitrate to seawater and you can cause a phytoplankton bloom. Yet the earliest cultures of Prochlorococcus lacked the genes necessary to assimilate nitrate; they required reduced forms of nitrogen, such as ammonia or nitrite, and some could not even use nitrite. This was a R448

sobering finding because the models of ocean productivity used to feed into global climate models assumed that all phytoplankton could use nitrate. Then along came Prochlorococcus, shattering the status quo. Eventually, however, we found some Prochlorococcus that could use nitrate, adding yet another layer to its diversity. Our challenge now is to figure out what selective pressures drove this diversification. Prochlorococcus is also pointing the way to our seeing entirely new features of ocean ecosystems. Recently, for example, we learned that they release lipid-bound vesicles containing DNA, RNA, and a host of other biomolecules into the surrounding seawater. This led to the discovery that many other marine bacteria are doing the same thing. What is the function of these vesicles? Is this one of the ways genes are being shuttled between different phyla? Prochlorococcus will soon provide clues, if not the complete answers. Finally, detailed analysis of the selective forces that drove evolution of metabolic diversity in Prochlorococcus has led to a general theory about the evolution of the biosphere. If the theory holds true, it will become clear that this tiny cell has played a disproportionate role in choreographing the history of the Earth. Where can I find out more? Biller, S.J., Berube, P., Lindell, D., and Chisholm, S.W. (2015). Prochlorococcus: The structure and function of collective diversity. Nat. Rev. Microbiol. 13, 13–27. Braakman, R. Follows, M.J., and Chisholm, S.W. (2017). Metabolic evolution and the selforganization of ecosystems. Proc. Natl. Acad. Sci. USA doi:10.1073/pnas.1619573114. Chisholm, S.W. (2012). Unveiling Prochlorococcus: The life and times of the ocean’s smallest photosynthetic cell. In Microbes and Evolution: The World That Darwin Never Saw, R. Kolter and S. Maloy, eds. (Washington, D.C.: ASM Press) p. 165. Flombaum, P., Gallegos, J.L., Gordillo, R.A., Rincón, J., Zabala, L.L., Jiao, N., Karl, D.M., Li, W.K., Lomas, M.W., Veneziano, D., et al. (2013). Present and future global distributions of the marine Cyanobacteria Prochlorococcus and Synechococcus. Proc. Natl Acad. Sci. USA 110, 9824–9829. Partensky, F. and Garczarek, L. (2010). Prochlorococcus: Advantages and limits of minimalism. Annu. Rev. Mar. Sci. 2, 305–331. Scanlan, D.J., Ostrowski, M., Mazard, S., Dufresne, A., Garczarek, L., Hess, W.R., Post, A.F., Hagemann, M., Paulsen, I., and Partensky, F. (2009). Ecological genomics of marine picocyanobacteria. Microbiol. Mol. Biol. Rev. 73, 249–299.

Massachusetts Institute of Technology, Cambridge, MA, 02139 USA. E-mail: [email protected]

Quick guide

Seabirds Stephen C. Votier* and Richard B. Sherley What makes a bird a seabird? Seabirds are entirely dependent on the marine environment for at least part of their lives (Figure 1). For some species this may be most of their life cycle, but it can be a very small part for others. The classification of seabirds is debated, but there are often thought to be around 350 species (~3.5% of all birds), across nine orders: Procellariiformes (albatrosses and petrels); Sphenisciformes (penguins); Gaviiformes (loons); Podicipidiformes (grebes); Anseriformes (waterfowl); Phaethontiformes (tropicbirds); Charadriiformes (gulls, skuas, skimmers, terns, phalaropes and auks); Pelecaniformes (pelicans); and Suliformes (frigatebirds, cormorants, gannets and boobies). Birds that occupy the littoral zone, for example, shorebirds and herons, are not usually considered seabirds. What characterizes seabirds? Despite their taxonomic diversity, seabirds share a number of convergent traits. Many have bet-hedging life history strategies characterized by extended immaturity, low reproductive investment spread over many years, and high adult survival. Albatrosses are famous for their longevity — the oldest known wild bird is Wisdom, a female Laysan albatross (Phoebastria immutabilis), banded as an adult in 1956 on Midway Atoll, Hawaii, and still breeding in 2017. Seabirds are also known for their ability to travel huge distances: Arctic terns (Sterna paradisaea) have the longest recorded migration of any animal, flying >80,000 km from Arctic breeding grounds to the Southern Ocean and back each year. Many species also regularly travel long distances between breeding and foraging grounds — northern gannets (Morus bassanus) may commute >30,000 km in search of food during a single season. Seabirds are also prodigious in their vertical movements — Emperor penguins (Aptenodytes forsteri) can dive to depths of >500 m, spending nearly 20 minutes underwater, while great frigatebirds (Fregata minor) have been recorded at altitudes of >4,000 m.

Current Biology 27, R431–R510, June 5, 2017 Crown Copyright © 2017 Published by Elsevier Ltd.