Volume 109, Issue 3 p. 363-365
ON THE NATURE OF THINGS: ESSAYS
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The photoaerogens: algae and plants reunited conceptually

William B. Sanders

Corresponding Author

William B. Sanders

Department of Biological Sciences, Florida Gulf Coast University, Ft. Myers, FL 33965-6565, USA

Correspondence

William B. Sanders, Department of Biological Sciences, Florida Gulf Coast University, Ft. Myers, FL 33965-6565, USA.Email: [email protected]

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First published: 07 March 2022
Citations: 2

Biology is replete with terminology that is sometimes excessive. But it is very difficult to assimilate and apply a concept for which no word exists. Strangely, this problem is at the center of the discipline of botany today. Introductory “plant diversity” courses and “plant biology” textbooks treat the algae as well as the embryophytes, and with good reason. Yet this broad collection of organisms with key features in common has no name. “Plant” is nowadays understood in a much narrower sense by most biologists since the term was repurposed to fit modern biosystematics. It can no longer be used broadly without an ad hoc definition (e.g., Palmer et al., 2004). The broader concept lost biosystematic status, appropriately enough, but not its biological significance: plants and all algae share unique features of tremendous importance that profoundly changed the entire course of evolution on the planet. And we know that these common features had a single origin (Delwiche et al., 1995; Tomitani et al., 2006; Ponce-Toledo et al., 2017; Sibbald and Archibald, 2020).

Abundant data, and the emergent consensus that systematics must reflect phylogeny, have long made it clear that the diverse organisms traditionally studied by botanists and phycologists belong in quite different domains, kingdoms, and supergroups. But another important line of phylogenetic research—into the origins of plastids—gives a contrasting perspective, one that interconnects this diversity horizontally across the major clades of life. Those investigations have clearly shown that the characteristic mode of nutrition shared by all algae and plants is not explained by convergence, but instead results from a common photosynthetic apparatus originating in cyanobacteria and repeatedly acquired laterally by eukaryotic lineages via endosymbiosis (Delwiche, 1999; McFaddin, 2001, 2014; Keeling, 2004, 2013; Archibald, 2009). While this unifying fact is well known, it has been far less integrated into the framework of botany than have the separating facts of phyletic diversity. We have the terminology to recognize the differences, but not the commonalities. To be able to consider all these organisms together, and emphasize the unique and significant features that they share in common, an inclusive term without taxonomic implications is needed.

As defined here, the photoaerogens encompass all lineages that inherited oxygen-generating photosynthesis. They are the cyanobacteria (blue-green algae), all eukaryotic algae, and the embryophytes. The eukaryotic clades inherited the cyanobacterial photosynthetic apparatus horizontally as well as vertically, with lateral transfer either directly from cyanobacteria or indirectly from other eukaryote lineages that had already acquired it (Figure 1). Although several distinct groups of bacteria evolved the means to harvest light energy in diverse ways, among them only the cyanobacteria use water as an electron-donor and generate molecular oxygen as a waste product (Hohmann-Marriott and Blankenship, 2011). None of the other lineages of photoautotrophic or photoheterotrophic bacteria has had a comparable impact on our planet and its biota, and none but the cyanobacteria are known to have passed on their photosynthetic apparatus laterally as organelles within the cells of diverse eukaryotes. The cyanobacteria are the sole originators of oxygenic photosynthesis (Delwiche et al., 1995). While biosystematics fully separates them from eukaryotic algae and plants, the phylogeny of plastids and the biology that goes with them link all these independent lineages together in a network of photoaerogenic organisms (Figure 1).

Details are in the caption following the image
Generalized tree of life outlined in grey, showing photoaerogenic lineages in color. Dashed lines indicate unresolved supergroup relationships at the root of eukaryote radiation. Horizontal double lines indicate lateral transfer into the cells of another lineage followed eventually by evolution into plastids integrated within the host. The chronological order of horizontal transfers shown is speculative or arbitrary. The number of such events resulting in plastids derived from red algal endosymbionts remains controversial. The dinoflagellates include a roughly equal number of photoautotrophs (or myxotrophs) with such plastids (characterized by the carotenoid peridinin), and heterotrophs that may depend metabolically upon the vestiges of those plastids inherited from photoautotrophic ancestors (Janouškovec et al., 2017). The remnant plastid of red algal origin found in apicomplexan parasites (Plasmodium, Toxoplasma) suggests that this heterotrophic clade likewise descends from related photoaerogen ancestors. Several dinoflagellate genera have more recently reacquired and integrated plastids of haptophyte (Karenia, Karlodinium), green algal (Lepidodinium) or diatom origin (Durinskia, Kryptoperidinium) by means of endosymbiosis or predation/kleptoplasty. The cryptophyte-derived plastids reported in some species of the dinoflagellate genus Dinophysis are most likely kleptoplastids temporarily retained from prey rather than permanent components of the host cell (Kim et al., 2012) and are not represented in the diagram. (Sources: Woese et al., 1990; McFaddin, 2001, 2014; Keeling, 2004, 2013; Archibald, 2009; Keeling and Burki, 2019; Sibbald and Archibald, 2020; Gabr et al., 2020)

The term photoaerogen is intended to be easily understood, clearly delimited, and reflective of the group's defining characteristics. Organisms that consume oxygen we call aerobic; those that generate oxygen are aerogenic. Algae and plants do so when they absorb light, therefore are photoaerogenic. They are also characterized by phototrophic nutrition and the pigment chlorophyll, but these are not defining characteristics, since several unrelated, non-aerogenic lineages of prokaryotes are also phototrophic and use chlorophylls (even chlorophyll a; Kobayashi et al., 2000). Within major lineages of photoaerogens, some subclades lost the photosynthetic mode of nutrition and therefore do not qualify as photoaerogens. The mycoheterotrophic angiosperm Monotropa is one example. There is nothing problematic about their exclusion; photoaerogens are not cladistically defined and need not include all descendants of a common ancestor. The term does not compete with biosystematic concepts, under which Monotropa is unequivocally placed in the Ericaceae among its photoaerogen relatives. In some animal and dinoflagellate species, aerogenic photosynthesis may be carried out by “kleptoplastids” harvested from digested photoaerogen prey and retained temporarily within host cells. As kleptoplastids are not integrated, heritable components of the host cell, those hosts would not be considered photoaerogens. However, there is reason to suspect that kleptoplastids acquired by the ancestors of some dinoflagellate genera may be the source of what have become the integrated plastids of certain contemporary lineages (Hehenberger et al., 2019).

The impact of oxygenic photosynthesis on the entire course of evolution cannot be overstated. The appearance, multiplication, and diversification of photoaerogens established new connections between the primeval food chain and an unlimited source of energy: solar power. The accumulation of molecular oxygen eventually transformed the ancient atmosphere from a reducing to an oxidizing one, setting the stage for the evolution of oxidative respiration. Aerobic organisms could use the reactive O2 to generate many times more ATP per carbohydrate molecule than otherwise possible, facilitating the rise of complex organisms with big energy budgets (Raymond and Segrè, 2006). The accumulation of oxygen as ozone in the upper atmosphere later provided the UV protection needed for the exposed continents to be colonized in a profuse diversification of terrestrial life. The photoaerogens are central to the history of life and are the inclusive subject of botany. If we wish to promote their integrated study and highlight the critical features they inherited from a common source, our language should make a place for them.

ACKNOWLEDGMENTS

This work was written during a sabbatic leave granted by Florida Gulf Coast University. The manuscript benefited from critical review by two anonymous referees.