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Microbial Endemism and Biogeography

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Microbial Endemism and Biogeography Microbial Diversity and Bioprospecting Edited by Alan T. Bull © 2004 ASM Press, Washington, D.C. Chapter 22 Microbial Endemism and Biogeography BRIAN P. HEDLUND AND jAMES T. STALEY THE MICROBIAL BIOGEOGRAPHY DEBATE Another reason to suppose that endemism exists for free-living microbes is that most plant, animal, The topic of microbial biogeography is almost and some fungal species arc endemic to one continent 100 years old, however, when confronted with ques­ or another. Indeed, examples of plant and animal tions about the existence and extent of endemism in families and even orders are known to be endemic to the microbial world, many microbiologists respond isolated islands (Brown and Lomolino, 1998). Fur­ with opinions and theoretical arguments rather than thermore, a basic tenet of biodiversity is that species examples of well-conducted studies. We begin this diversity increases with decreasing body size (May, chapter with an overview of this debate as it ·applies 1988, Wilson, 1992). For terrestial animals, each 10- to free-living prokaryotes in part because there are fold reduction in body length or 1,000-fold reduction relatively few good microbial biogeography studies. in body weight corresponds to roughly a 100-fold in­ Furthermore, the arguments help to frame microbial crease in species diversity (May, 1988). If such a rela­ biogeography in the larger context of biodiversity in tionship held for microbes, the number of microbial that if endemism is common, then many more species species on our planet would be astronomical and it exist. would seem that many microbes would have to be en­ demic to achieve this level of diversity. However, it is The Argument for Microbial Endemism important to clarify that there is no theoretical ground for extrapolating a species richness-"body" Arguments for endemism among free-living mi­ size correlation to include microbes, and the current crobes generally draw from examples of endemism of lack of a meaningful species definition for most mi­ other organisms. First, any international traveler crobes reduces any such relationship to a conceptual knows that many pathogenic microbes, both viral level rather than a truly quantitative level. Neverthe­ and bacterial, have distinct biogeographies. For ex­ less, given that endemism is the norm, why should ample, dogs and cats entering Australia are quaran­ free-living microbes defy this pattern? tined in order to prevent the introduction of the rabies virus onto the continent. And historians are The Argument for Microbial Cosmopolitanism quick to point out one of the great tragedies in human history, the re-peopling of the Americas by Euro­ The cosmopolitan view of the microbial world peans, who brought many newpathogens with them has a long history (Baas-Becking, 1934) and has with­ to the new world. This mi~robial invasion included stood the test of time relatively well. Although some the variola virus (sm'allpox),themeasles virus, the in­ pathogens provide fuel for the endemism argument, fluenza viru~, the yellow fever virus, Salmonella ty­ others are clearly cosmopolitan, consisting of a lim­ pha; (typhoid fever), Vibri; cholerae ·(cholera), and ited number of globally distributed clonal lineages, Yersinia pestis (plague) and resulted inthe infection including Escherichia coli, Haemo[Jhi!us influenzae, and death of >95% of the pre~Columbian native Neisseria meningitidis, Staphylococcus aureus, and population (Diamond, 1999). The fact that some Streptococcus pneumoniae. Appropriately, Cho and pathogens have distinct biogeographies may suggest Tiedje (2000) have pointed out that these bacteria are that solTie free~living microbes have biogeographies closely associated with humans and their biogeogra­ as well. · " .· .· phies are inevitably affected by human activity, but it Brian P. Hedlund • De~art'~ent of Bi~logi;:al Sci~~c~s, University of Nevada, Las Vegas, 4505 Maryland Parkway, Las Vegas, NV 89154-4004. James T. Staley • Department of Microbiology, University of Washington, Seattle, WA 98195-7242. "225 226 HEDLUND AND STALEY could be argued that free-living microbes are also dis­ ' ' ' persed by human activities, leading to cosmopoli­ ' ' ' tanism, as is also true of many plants and animals. ' ' ' The cosmopolitan view has recently been ' ' staunchly advocated by the eukaryotic microbial ' ' ? ' ' ecologist Finlay, among others, who has published • ' frequently in high-profile journals (Finlay, 2002; ' ' Finlay and Clarke, 1999; Finlay et a!., 1996). The argument states that small body size and immense population size lead to constant dispersion of mi­ t crobes by a variety of mechanisms (including hu­ ~I mm man-mediated) and, consequently, cosmopolitanism. Log (length) Some microbes form cysts or spores that are partic­ ularly well suited for long-term survival during pas­ Figure 2. Conceptual figure showing the enormous effect of bio­ sive dissemination, and even microbes that do not geography and body size models on biodiversity estimates. Ac­ form specific survival stages are known to survive cording to Finlay's model (2002), most of the species diversity on this planet would be in the size range of small insects (solid line). long periods in metabolically inactive states. These Alternatively, extrapolation of the body size and species diversity microbtal seeds "bloom" when and where condi­ relationship (May, 1988) to include microbes would yield a vastly tions favor their growth. greater number of prokaryotic species (dotted line). In reality mi­ Based on these ideas and corroborating data on crobtal diversity may lie between the two extremes (question the cosmopolitanism of many protist morphospecies, mark). Finlay (2002) has proposed that an ubiquity and bio­ diversity transition occurs at a body length of be­ tween 1 and 10 mm. According to this model, essen­ They also clarify how little we know. Figure 1 tially all species with body lengths larger than this shows Finlay's model (2002) of microbial biogeog­ transition size have distinct biogeographies, whereas raphy (solid line), which invokes that essentially all essentially all organisms smaller than the transition prokaryotes are cosmopolitan. Although Finlay is size are ubiquitous (i.e., cosmopolitan). dogmatic about this view, we believe that it is far These arguments draw attention to the topic of from conclusive and present it here as a conceptual microbtal biogeography and help to set conceptual extreme in favor of microbial cosmopolitanism. The limits on microbial biogeography and diversity. opposing extreme (dotted line) is that nearly all or­ ganisms have meaningful biogeographies at some taxonomic level, regardless of size. We believe it is ..s 100 important that microbiologists discuss, and eventu­ ·~ Ul (\) --------------- Ul ·~ ally work toward resolving, the microbial biogeog­ (\)...:::: 80 ·-(.) 0..ell raphy debate because it has great implications for (\) bh ~0 our understanding of biodiversity (Fig. 2). If Finlay 4.; (\) 60 0 bll is correct, then microbes are not particularly diverse <1) .9 ? bll..C 40 • (solid line). On the other hand, if microbial en­ ..... ~"' g demism is the norm, then the majority of diversity ~ ·.;:: 20 .... Ul (\) ·~ on our planet is microbial (dotted line). In the fol­ t=l-.'"0 0 lowing sections we discuss some studies on micro­ t bial biogeography, which seem to suggest that Fin­ ~1 mm lay's view may be correct on a certain taxonomic Log (length) level-the protist morphospecies or the prokaryotic genus-but that some microbes have meaningful Figure 1. Conceptual figure showing alternative biogeography and biogeographies below that level. body size models. Finlay (2002) has proposed that an ubiquity and bmdiverslty transition occurs at a body length of 1 to 10 mm, whtch suggests that many protozoa and nearly all prokaryotes are cosmopolitan (solid line). Alternatively, the apparent ubiquity and ARE MICROBIAL EUKARYOTES REALLY biodiversity transition may represent the size at which the mor­ COSMOPOLITAN, OR DO WE NEED A phospecies concept decays, and future molecular studies iuay show BETTER MAGNIFYING GLASS? that most mtcrobial species have distinct biogeographies, as do larger organisms (dotted line).lt is likely that the percentage of mi­ crobes with distinct biogeographical patterns lies somewhere be­ The biogeography of free-living microbial eu­ tween the two extreme models (question mark). ' karyotes hasreceived a lot of attention; therefore it is -,. ~ ' ;, CHAPTER 22 • MICROBIAL ENDEMISM AND BIOGEOGRAPHY 227 significant that protozoologists seem to agree that to resolve morphologically similar (or identical) most protist morphospecies are cosmopolitan. To il­ species that breaks down with decreasing size? It lustrate this axiom, Finlay and Clarke (1999) used seems obvious that at some size or morphological transmission electron microscopy to survey 25.2 1-1l of complexity limit, the morphodiversity concept should superficial sediment from Priest Pot, a small freshwa­ give way to a more sensitive and less subjective ter pond in the United Kingdom. In this tiny sample molecular phylogenetic diversity concept. Perhaps they observed siliceous scales representing 32 of Wilkinson has described this limitation rather than a the 41 known morphospecies of the ciliate Para­ true biogeographical pattern. Likewise, Finlay's ubiq­ physomonas. In addition, they found that the most uity and biodiversity transition may instead be the numerous Paraphysomonas species in Priest Pot were morphodiversity-molecular phylogenetic diversity also
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