Abstract

In the 1970s, R.D. MacElroy coined the term ‘extremophile’ to describe microorganisms that thrive under extreme conditions (MacElroy 1974). This hybrid word transliterates to ‘love of extremes’ and has been studied as a straightforward concept for the past 40 years. In this paper, we discuss several ways the term has been understood in the scientific literature, each of which has different consequences for the distribution and importance of extremophiles. They are, briefly, Human-Centric, at the Edge of life’s habitation of Morphospace, by appeal to Statistical Rarity, described by Objective Limits, and at the Limits of Impossibility for metabolic processes. Importantly, these concepts have co-existed, unacknowledged and conflated, for decades. Confusion and equivocation threaten to follow from the wildly varied inclusion or exclusion of organisms as extremophiles depending on the concept used. Under some conceptions, entire kinds of extremophiles become meaningless. Since our understanding of how life works is shaped by what we take to be its extremes, clarifying extremophily is key for many large-scale projects in biology, ecology, biotechnology and astrobiology. In what follows, we proceed as if a noncontroversial account of life is possible and that it is possible to find complex chemistry in the Universe that is similar enough to Life on Earth such that both may be considered instances of ‘life’ (but see Mariscal & Doolittle 2018). We raise, but do not address, the questions of whether the distribution of Life on Earth is representative of what we may find elsewhere in the Universe, whether the same kinds of extremophiles would exist given a replay of the tape of life. Additionally, each of these concepts assumes life based on some sort of biochemistry in this universe, effectively setting aside claims made by some artificial life proponents that their digital organisms are genuine examples of life (Langton 1989, Ray 1995). On the distinction between extremophilic and extremotolerant, we note that all accounts accept the latter as a broader category than the former, since ‘phily’ means love and tolerance is a prerequisite for love under any conception. Indeed, there will be many extremely impoverished environments where tolerance is the only option and thriving is precluded, e.g. Bacillus marismortui was extracted and grown from 250-million-year-old salt crystals in the Permian Salado Formation in an inactive yet persistent state (Vreeland et al., 2000). We also note that extremophily, as a functional category, is potentially applicable at many levels of the biological hierarchy. Extremophily at one level does not necessarily extend to higher and lower levels. For instance, a microorganism in isolation might be quite intolerant to certain environmental conditions yet flourish when subjected to the same conditions as a community or natural biofilm. Alternatively, a protein molecule might be quite stable or active under certain conditions even if the optimal environment for the organism containing it is far more mesophilic. There is an industry of artificially selecting organisms and proteins to adapt to extreme environments (see van den Burg & Eijsink 2002), providing some justification to consider ‘functioning at extremes’ as a worthwhile category of investigation. Finally, we also note certain physico-chemical ranges are rarely considered with respect to extremophily – timespan, size, nutrient availability (Hoehler & Jørgensen 2013), etc. – as well as some biological parameters – abundance, isolation, competition, etc. Perhaps scientific interest must also come into play as to the reason these criteria are not considered relevant. We return to this issue later. In the next section, we give five definitions of extremophily, show their benefits, drawbacks, and unintended yet unavoidable consequences. These arguments are summarized in Table 1 and represented visually in Figures 1 and 2. Given research on polyextremophiles, it seems Figure 2 is a more plausible representation of the state of current knowledge than Figure 1 (Harrison et al. 2013). Life is patchily distributed across various dimensions, which may reflect its contingent history, poor sampling, or (perhaps) fundamental limits. Figure 3 shows the conceptual flowchart for all of these views. In the following section, we take a step back to ask whether we should choose between these definitions and how such a judgment could be made. We argue for a limited pluralism, in which some, but not all, of the concepts are acceptable relative to certain practical and theoretical aims.