The disadvantages of current proposals to redefine lichens

Lichen-forming fungi and their algal symbionts together produce composite thalli that often have the appearance and properties of unitary organisms. Although the exact contours of the concept may vary according to viewpoint, lichens have been commonly distinguished from other fungal–algal symbioses by a useful and widely cited definition (Hawksworth, 1988; Hawksworth & Honegger, 1994), wherein the mycobiont comprises the external component (exhabitant) that houses the interior but extracellular algal symbiont(s). More recently, increased attention has been focused on additional microorganisms, particularly fungi and bacteria, that form part of the lichen thallus microbiome (Grube et al., 2015; Spribille et al., 2016; Cernava et al., 2017; Smith et al., 2020; Tzovaras et al., 2020; Cometto et al., 2022). This has revealed a new dimension to lichen biology, similar to that recognizable in plants and animals as the diverse microbial inhabitants of their internal and external surfaces are explored (Porras-Alfaro & Bayman, 2011; Ezenwa et al., 2012; Gilbert et al., 2018). Such research highlights the degree to which biological communities coexist at very different scales. A plant, an animal, and a lichen thallus are all components of a broader community of interacting macro-organisms, while at a finer level of organization, each may individually harbor its own microbial community or communities. Although microbiome research has changed how we think about plants and animals, it has not resulted in any effort to redefine them. By contrast, a number of lichen biologists have recently proposed expanding the definition of a lichen to include other microorganisms that colonize the thallus. These proposals, and indeed the question of whether a new definition is warranted or desirable, ought to be considered critically. Hawksworth & Grube (2020) redefine a lichen as an ecosystem formed by the interaction of an exhabitant fungus, its photosynthetic partners, and an indeterminate number of other microorganisms. This new interpretation elevates microbiome inhabitants to a defining status equivalent to that of the mycobiont and photobiont(s), even though their roles and significance are still poorly understood and their critical importance to the symbiosis far from proven. It merges the lichen and its microbiome into one and the same concept, a treatment not suffered by the plant or the animal. Of course, as Lücking et al. (2021) point out, the lichen's relationship to its microbiome might be viewed differently, since, unlike the plant or animal, a lichen is already defined as a partnership of organisms. But consider the mycorrhiza, a symbiosis to which lichens are frequently compared. The rhizosphere/hyphosphere likewise harbors diverse microorganisms that can make significant contributions to the symbiosis (e.g. Wang et al., 2023) yet still do not figure in the definition of a mycorrhiza. The omission of these associates does not imply that they are unimportant. It merely indicates that the core relationship between fungus and photoautotroph remains a meaningful concept in itself, one that biologists prefer not to lose. Structurally and physiologically, lichen symbionts are quite intimately associated; photobionts are induced to release massive amounts of carbohydrate (Richardson et al., 1968; Smith, 1980), which is channeled apoplastically to the mycobiont by pathways sealed with fungus-derived hydrophobic materials (Honegger, 1991; Trembley & Honegger, 2002). At present, there is no reason to believe that any other thallus inhabitant has a comparable degree of integration, even if some might provide important services. It is the structure and interaction of mycobiont and photobiont that create the physical habitat within which the associated microorganisms dwell. If it can be demonstrated that additional microorganisms are essential to the transformative development of the lichen thallus, then their inclusion in the definition might be justified. Such an argument was proposed for cyphobasidialean yeasts that may associate with certain macrolichens (Spribille et al., 2016), but follow-up studies found low co-occurrence (Lendemer et al., 2019; Smith et al., 2020) or far lower specificity to the mycobiont proper than that shown by the lichen photobionts (Mark et al., 2020). Hawksworth & Grube (2020) are appropriately cautious in their treatment of claims that additional microbiome members may be essential or co-equal partners in the lichen symbiosis. It therefore comes as a surprise that they feel the definition of a lichen needs to be amended. In redefining the lichen as an ecosystem, Hawksworth & Grube (2020) implicitly expand the lichen concept even further. The proposal that lichens be considered ecosystems appears to have originated with Farrar (1976), although that author did not believe there was evidence that any other organisms were partners in the lichen symbiosis besides the principal fungal and algal symbionts. In recent years, application of the term ecosystem to individual thalli has become more common as the diversity of the lichen microbiome is increasingly appreciated (Grube et al., 2009; Cardinale et al., 2012; Pankratov et al., 2017; Škvorová et al., 2022). But this usage does not seem to take into account the definition of ecosystem, which refers to a level of organization above that of the community. The term was coined (by the founder of the New Phytologist) to explicitly include the key components of the physical and chemical environment together with the biotic communities they sustain (Tansley, 1935). Contemporary ecology textbooks maintain this usage (e.g. Ricklefs, 2008). To define a lichen as an ecosystem – a micro-ecosystem – would therefore require inclusion of the mineral, soil or plant substratum upon or within which the lichen grows, at the very least. While such elements are clearly relevant to lichen biology, the utility of making them defining features is questionable. For most biologists, a lichen removed from its substratum is still a lichen. Other modifications were proposed by Lücking et al. (2021), who provide a summary of previously published lichen definitions and an extensive discussion of criteria. Their definition makes no reference to ecosystems, and the microbiome members they would add to the lichen concept are limited to those fungi and bacteria that might be regarded as ‘obligately associated’. But obligate for whom: the associated organism or the lichen symbiosis? Most, if not all, lichen photobionts are themselves not obligately associated with lichen-forming fungi, even if the symbiosis improves their odds of survival in many microhabitats. Without them, however, you do not have a lichen. On the other hand, the question of whether any other microorganisms are essential to the mycobiont–photobiont partnership remains unresolved at present. The Lücking et al. (2021) definition also refers to the primary mycobiont as a fungus or a fungus-like organism, apparently in deference to the theoretical possibility that an oomycete–algal symbiosis might exist or have existed and could conceivably fit the criteria for lichenhood. These extensions of the lichen concept take plausible but entirely hypothetical cases and integrate them into the definition of a lichen. With that comes a significant risk of circular reasoning. If we intend to critically examine whether or not lichen symbioses involve other indispensable participants, or mycobionts that are not true fungi, it is counterproductive to work with a lichen concept that has already recognized these hypotheticals as defining features. A further proposal to ‘reconceptualize lichen symbioses’ has also been published (Allen & Lendemer, 2022), but its authors do not explicitly suggest any changes to the definition of a lichen. Because the myriad variations on every theme in the natural world rarely fit neatly into human conceptual schemes, most biological definitions are imperfect, arbitrary, and/or amended with exceptions. Their utility is what matters. It has so far proven useful to distinguish microbiome elements from the biological macrostructure that creates habitat for them. If lichen is redefined more broadly to encompass additional organisms that form part of the thallus microbiome, not to mention the physical factors that support the community, no term remains to refer specifically to the symbiotic partnership between mycobiont and photobiont. Before we dissolve this fundamental concept into a broader one with more nebulous boundaries, there should first be convincing indications that it is obsolete. A new, broader concept can always be accommodated by a different term (e.g. lichen holobiome); it need not replace the current one. The fact that lichens, like mycorrhizas, harbor a diverse microbiome, some of whose members might make significant contributions to the symbiosis, does not in itself mean that the mycobiont–photobiont concept is obsolete. All but a minuscule fraction of a healthy lichen's biomass (excepting those embedded within their substratum) consists of mycobiont and photobiont and the materials they produce. Just what sorts of microorganisms comprise the remainder, and what roles they might play, are currently the subjects of much interesting research. But at present there is no evidence that any microbiome element has the essential status of the core components. Subtract the mycobiont or photobiont, by contrast, and lichen identity is clearly lost. They are the defining elements, at least for now. The author thanks Drs Sergio Pérez Ortega and Raquel Pino Bodas for helpful discussion of this topic. The manuscript benefited from critical review by two anonymous referees. None declared.