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Acidophile Microbiology in Space and Time

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Acidophile Microbiology in Space and Time Acidophile Microbiology in Space and Time D. Barrie Johnson 1 and Raquel Quatrini 2,3,4 1 School of Natural Sciences, Bangor University, Bangor, LL57 4UW, UK 2 Fundación Ciencia and Vida, Santiago, Chile 3 Universidad San Sebastian, Santiago, Chile. 4 Millennium Nucleus in the Biology of Intestinal Microbiota, Santiago, Chile. DOI: https://doi.org/10.21775/cimb.039.063 Abstract Tis article introduces the subject of acidophile Te study of extreme acidophiles, broadly defned microbiology, tracing its origins to the current status as microorganisms that grow optimally at pH values quo, and provides the reader with general information below 3, was initiated by the discovery by Waksman which provides a backdrop to the more specific and Jofe in the early 1900s of a bacterium that was topics described in Quatrini and Johnson (2016). able to live in the dilute sulfuric acid it generated by oxidizing elemental sulfur. Te number of known acidophiles remained relatively small until the second half of the 20th century, but since then Acidophilic microorganisms has greatly expanded to include representatives defned of living organisms from within all three domains Acidophiles are broadly defned as life forms that of life on earth, and notably within many of the grow preferentially in natural or man-made envi- major divisions and phyla of Bacteria and Archaea. ronments where the pH is well below 7. Together Environments that are naturally acidic are found with other categories of ‘extremophiles’, they have throughout the world, and others that are man- greatly expanded our knowledge of the diversity of made (principally from mining metals and coal) life, our understanding on how microorganisms can are also widely distributed. Tese continue to be adapt to seemingly hostile situations, and provided sites for isolating new species, (and sometimes new scenarios for the possibility that life forms similar genera) which thrive in acidic liquor solutions that to those that colonize inhospitable niches on Earth, contain concentrations of metals and metalloids our own planet, may be found on planets and satel- that are lethal to most life forms. Te development lites within and outside of our solar system. and application of molecular techniques and, more While there is no formal defnition of what con- recently, next generation sequencing technologies stitutes an acidophile, one proposed by Johnson has, as with other areas of biology, revolutionized (2007) has gained general acceptance. Tat deline- the study of acidophile microbiology. Not only ated ‘extreme acidophiles’ as those that have pH have these studies provided greater understanding optima at 3 or below, and ‘moderate acidophiles’ as of the diversity of organisms present in extreme those with pH optima of 3–5, though some species acidic environments and aided in the discovery are capable of growing at pH < 3. Acid-tolerant spe- of largely overlooked taxa (such as the ultra-small cies have pH optima above 5, though they can grow uncultivated archaea), but have also helped uncover at pH values lower than this. Te most acidophilic some of the unique adaptations of life forms that of all known life forms (the euryarchaeote Picrophi- live in extremely acidic environments. Tanks to lus, which currently contains two validated species) the relatively low biological complexity of these has a pH optimum of 0.7 and can grow at pH 0. ecosystems, systems-level spatio-temporal studies Given that pH is a logarithmic scale, this means of model communities have been achieved, laying that Picrophilus spp. can grow in liquors where the + the foundations for ‘multi-omic’ exploration of hydronium ion (H3O ) concentration is 50–100 other ecosystems. times greater than that tolerated even by many caister.com/cimb 63 Curr. Issues Mol. Biol. Vol. 39 Johnson and Quatrini extreme acidophiles. Te term ‘hyper-acidophiles’ of microorganisms being detected in extremely (analogous to ‘hyper-thermophiles’ which was low pH, as in other environments. Improved and introduced when prokaryotes that had temperature probably novel cultivation-based approaches and optima > 80°C were discovered, some of which techniques are currently required to catch up and grew well above 100°C) is a more appropriate way keep pace with what cultivation-free studies are to describe species that grow optimally at pH < 1, revealing about the biodiversity of extreme envi- though such prokaryotes appear at present to be ronments, including those that are extremely acidic. very rare. Te same general rule applies with pH as other environmental parameters (temperature, salinity, Nature, genesis, and global pressure, etc.) which is that, as the stress factor distribution of extremely acidic (in this case, acidity) increases in intensity, so the environments number of species that can tolerate or grow in such Extremely acid environments can vary greatly in environments decreases. Extreme acidophiles are scale, nature and origin. Gastric acid produced in exclusively microbial. Macroscopic life forms are the lining of the human stomach has a pH of ~1.5 to sometimes found in low-pH environments, such as 3.5 due to the production of hydrochloric acid. In the angiosperms Erica spp. that grow in acidic soils contrast, in both man-made and natural extremely and Juncus bulbosus which can colonize the fringes acidic environments, sulfuric acid is usually the of acidic pit lakes. However, cell membranes of mineral acid responsible for the low-pH conditions. higher plants are susceptible to damage at pH < 4, In situations where low pH is due to the presence of and the roots of wetland plants such as Juncus spp. organic acids, such as humic acids/colloids (as in are generally found in the sediments of acidic ponds acid peats) these tend to be moderate (>3) rather and lakes where the pH is signifcantly greater than than extreme. Notable exceptions are the pH of that of the water body itself. While it is the case lemon and lime fruits, which have pH between that most extremely acidophilic eukaryotes are 2 and 3 due to their elevated concentrations of unicellular, some multicellular life forms, including undissociated citric acid (a tricarboxylic acid with rotifers and some crustaceans, can thrive in some pKa values of 3.1, 4.8 and 6.4). low-pH environments. Acidophiles are also widely Many biological processes, for example fer- distributed in the ‘tree of life’, occurring in all three mentation, generate acidity due to the production domains of life, Bacteria, Archaea and Eukarya, and of small molecular weight aliphatic acids (such within multiple phyla in the same domain (Fig. 1.1). as lactic and propionic acids) as metabolic waste See also Quatrini and Johnson (2016). products. Acetogenic bacteria have long been used Te number of species of extremely acidophilic to generate malt and wine vinegars, which have pH microorganisms that have been isolated and char- values of ~2.5. However, biological processes that acterized has increased almost exponentially from generate mineral (inorganic) acids have, at least in just two in the mid-20th century to > 50 in the early theory, greater potential for generating extremely 21st century. It is now clear that, as a group, acido- low-pH environments due to the generally lower philes are highly heterogeneous from physiological pKa values of the acids involved. Nitrifcation is a and metabolic perspectives, and can utilize difer- two-stage oxidative process that generates nitrous ent sources of energy (solar, organic and inorganic (pKa 3.4) and nitric (pKa −1.6) acids. However, the chemicals), electron acceptors (oxygen, ferric iron vast majority of prokaryotes that catalyse these dis- and sulfur) and carbon sources (organic, inorganic, similatory reactions (mostly chemolithotrophs) are or both) although some metabolic functions seem acid sensitive and only thrive in environments that to be rare (e.g. fermentation) or absent (e.g. dissimi- are self-bufered, such as marine waters and non- latory nitrate reduction), and chemolithotrophy acidic soils. In contrast, the dissimilatory oxidation unusually commonplace amongst acidophilic of elemental and reduced forms of sulfur is car- microorganisms (Johnson and Aguilera, 2015). ried out by prokaryotes that have widely diferent Te evolution and now routine application pH ranges and optima for growth, and includes a of molecular techniques for studying biological number of species of extremely acidophilic bacteria systems has resulted in many uncultivated species and archaea. caister.com/cimb 64 Curr. Issues Mol. Biol. Vol. 39 Figure 1.1 Phylogenetic tree of bacterial and archaeal phyla based on the 16S small subunit rRNA gene sequence, constructed as described in Quatrini and Johnson (2016). taxonomic groups are defned by the clade colour index at the right side of the fgure and the presence of acidophiles in each clade is indicated in pink. Metabolic properties of each group of acidophiles are defned by the coloured circles outside the tree (coded as in the left side index). The fgure was prepared by Juan Pablo Cárdenas (Fundación Ciencia and Vida and Universidad Andres Bello, Santiago, Chile). caister.com/cimb 65 Curr. Issues Mol. Biol. Vol. 39 Johnson and Quatrini Sulfur is one of the more abundant elements in be conducive to the (microbial) oxidation of the the lithosphere, occurring at ~0.05% on a weight reduced sulfur, which usually (though not neces- basis. It is also a complex element, and can exist in sarily) requires the presence of oxygen, and (iii) the up to nine diferent oxidation states ranging from acidity generated needs to exceed the neutralizing −2 (e.g. in hydrogen sulfde; H2S) to +6 (e.g. in the capacity of the niche in which it is occurring. Geo- 2– sulfate anion; SO4 ; Steudel, 2000). Catenation thermal sites ofen fulfl all three criteria. Crystals of (the ability of sulfur atoms to bond to each other prismatic sulfur can form in the vents of volcanoes to form chains of practically unlimited lengths) is from the condensation of sulfur dioxide and hydro- another characteristic of this element.
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