Archea Diversity PDF

17 Diversity of Archaea I Euryarchaeota 594 II Thaumarchaeota and Cryptic Archaeal Phyla 603 III Crenarchaeota 608 IV Evolution and Life at High Temperature 614...

17 Diversity of Archaea I Euryarchaeota 594 II Thaumarchaeota and Cryptic Archaeal Phyla 603 III Crenarchaeota 608 IV Evolution and Life at High Temperature 614 MICROBIOLOGYNOW Methanogens and Global Climate Change A diversity of methanogens exists within the domain of methane. These two agricultural activities alone account Archaea. Methanogens are among the oldest microbes on for a major fraction of global methane emissions. Remark- Earth and have a tremendous impact on our biosphere. ably, however, human activities have even created new Methanogens in nature promote the anaerobic decomposi- habitats for methanogens under glaciers. The meltwater tion of organic matter by consuming the products of from this Greenland glacier (photo) is supersaturated with fermentative and syntrophic metabolisms. Methanogens methane and contains DNA from cells of the Methanomicro- release methane as a waste product, and this methanogen- biales, Methanosarcinales, and Methanobacteriales, highly esis is a natural part of Earth’s carbon cycle. However, diverse groups of methanogens. As climate change acceler- atmospheric methane has been increasing dramatically since ates glacier melting, the meltwater makes available ancient the dawn of the industrial age. Methane, like CO2, traps heat organic carbon buried beneath the ice. This meltwater in the atmosphere, contributing to the greenhouse effect. creates large subglacial wetlands that are rapidly colonized However, molecule for molecule, methane traps far more by cold-active methanogens. heat than does CO2. Moreover, whereas the increase in Massive amounts of organic carbon have been locked atmospheric CO2 comes mostly from burning fossil fuels, away for eons in frozen Arctic soils. As temperatures on the increase in atmospheric methane comes mostly from Earth increase, this carbon thaws, creating new habitats for human activities that promote methanogenesis. methanogens. Thus, accurately predicting the consequences Human activities have created many new opportunities of global climate change will require us to understand me­ for methanogens. In particular, domesticated ruminants such thanogen diversity and how humans affect it. as cows, sheep, and goats harbor methanogens within their rumens. In addition, during rice production, farmers flood the Source: Lamarche-Gagnon, G., et al. 2019. Greenland melt drives con- tinuous export of methane from the ice-sheet bed. Nature 565: 73. soil, generating artificial wetlands that release huge amounts 592 M17_MADI4790_16_GE_C17.indd 592 04/03/2021 20:43  CHAPTER 17 Diversity of Archaea  593 The domain Archaea is named for the Archaean eon, the period of representatives of the DPANN, TACK, and Asgard groups (Figure 17.1) geological history when life first spread across Earth (◀ Figure 13.1). have been discovered relatively recently. In the Archaean, high temperatures and an atmosphere devoid of While all Archaea share certain features, this domain encompasses O2 and thick in toxic gases enveloped Earth. Archaea were once considerable physiological diversity. Common traits of all Archaea thought to be remnants of this forgotten age since many Archaea live include ether-linked lipids, a lack of peptidoglycan in cell walls in extreme environments such as volcanic systems or salt ponds. We (Chapter 2), and structurally complex RNA polymerases that resemble now know, however, that Archaea occupy a wide range of habitats those of Eukarya (◀ Section 6.6). These features were likely present in and they perform important biogeochemical reactions in soil, the the last common ancestor of the Archaea. Genomic analyses suggest oceans, wetlands, and even in the guts of animals. While Archaea that the earliest Archaea lived at high temperature, oxidized H2 as an and Bacteria are both single-celled organisms with prokaryotic cell energy source, and fixed CO2 using the reductive acetyl-CoA pathway structure (Chapter 2), these domains are highly differentiated both (◀ Section 14.14 and Figure 14.34). Despite their shared phylogenetic genetically and physiologically. In many ways, Archaea share more origin, contemporary species of Archaea are metabolically diverse. features with Eukarya than with Bacteria. Indeed, it is likely that Archaea can be chemoorganotrophs or chemolithotrophs, they can be archaeal cells contributed fundamentally to the origin of the domain respiratory or fermentative, and they can be aerobic or anaerobic using Eukarya (◀ Section 13.4 and Figure 13.10). In this chapter, we will a wide diversity of electron donors and acceptors (Chapter 14). learn about the enormous phylogenetic and physiological diversity In addition, certain physiological capabilities are uniquely found found within the domain Archaea. within the domain Archaea. Methane production, for example, is a The Archaea are nearly as diverse as the Bacteria, but the vast unique characteristic of Archaea called methanogens (◀ Section 14.15, majority of Archaea have thus far proven difficult to grow in cul- Figures 14.38 and 14.39). Methanogenesis evolved very early within ture. Hence, it is likely that we still have much to learn about the the archaeal domain, and all well-characterized methanogens belong breadth of characteristics in organisms in this domain. To date, to the phylum Euryarchaeota. Methanogenesis is a globally important most well-characterized species of Archaea come from only two process that has produced virtually all of the natural gas on Earth and phyla: the Euryarchaeota and the Crenarchaeota (Figure 17.1). In addi- has a significant effect on climate because methane is a strong “green- tion, several species have been isolated from the phylum house gas” ( ▶ Sections 21.1, 21.2; and see page 592). Archaea are also Thaumarchaeota. By contrast, the phyla Korarchaeota and Nanoar­ well known for containing many examples of extremophiles 4 UNIT chaeota are represented only by strains grown in coculture or stud- (◀ Section 1.5 and Table 1.2) including hyperthermophiles ied using enrichment techniques (▶ Section 19.1). The use of (organisms with growth temperature optima above 808C), as well metagenomics (◀ Section 10.7) and single-cell genome sequencing as halophiles, acidophiles, and psychrophiles (Chapter 4). (◀ Section 10.11) has led to an explosion in our understanding of With this brief background and the phylogeny of Archaea firmly the phylogenetic and physiological diversity of the archaeal in mind (Figure 17.1), we now consider the organismal diversity of domain. As a result, many new phyla of Archaea such as this fascinating domain of life. Nanoarchaeota Euryarchaeota Thaumarchaeota Crenarchaeota Korarchaeota Natrialbales Haloferacales Nitrosopumilales Cenarchaeales Metanonatronarchaeales Halobacteriales Methanomicrobiales Methanobacteriales Aigarchaeota Nitrososphaerales Methanocellales Methanopyrales Methanosarcinales Desulfurococcales Archaeoglobales Methanococcales Thermoproteales Thermoplasmatales Bathyarchaeota Sulfolobales Methanomassiliicoccales Korarchaeales Thermococcales TACK Asgard Archaea Nanoarchaeales DPANN Root Figure 17.1 Schematic representation of the phylogeny of the major taxonomic orders within the domain Archaea. Five major archaeal phyla (studied in pure or highly enriched cultures) and their most representative orders are indicated in color, while other archaeal taxa are indicated in black. While archaeal phyla are nearly as numerous as Bacteria, far fewer Archaea have been cultivated. Archaeal phyla can be organized into four major branches, or superphlya, consisting of the Euryarchaeota, DPANN (represented here by Nanoarchaeota, see Section 17.6), TACK (composed of Thaumarchaeota, Aigarchaeota, Crenarchaeota, Korarchaeota, and related lineages, see Section 17.8), and Asgard Archaea (see Section 17.8). The root of the archaeal tree lies between these four branches though the exact position remains uncertain. M17_MADI4790_16_GE_C17.indd 593 04/03/2021 20:43  594   UNIT 4 MICROBIAL DIVERSITY I Euryarchaeota 17.1 Extremely Halophilic Archaea T he phylum Euryarchaeota contains most cultured species of Archaea. The group is metabolically diverse and includes methanogens, halophiles, thermophiles, and hyperthermophiles. KEY GENERA: Halobacterium, Haloferax, Natronobacterium Extremely halophilic Archaea, often given the nickname “haloar- chaea,” are a diverse group that inhabits environments high in salt. These include naturally salty environments, such as solar salt E uryarchaeota comprise a large and physiologically diverse group of Archaea. This phylum includes methanogens as well as many genera of extremely halophilic (salt-loving) Archaea. As a evaporation ponds and salt lakes, and artificial saline habitats such as the surfaces of heavily salted foods, for example, certain fish and meats. Such salty habitats are called hypersaline study in physiological contrasts, these two groups are remarkable: (Figure 17.2). The term extreme halophile is used to indicate that Methanogens are the strictest of anaerobes while extreme halophiles these organisms not only are halophilic but require a very high are primarily obligate aerobes. Other groups of Euryarchaeota include level of salt, in some cases at levels near saturation (◀ Section 4.15 the hyperthermophiles Thermococcus and Pyrococcus, the hyperther- and Figure 4.27). mophilic methanogen Methanopyrus, and the cell wall–less Thermo­ An organism is considered an extreme halophile if it requires 1.5 M plasma, an organism phenotypically similar to the mycoplasmas (about 9%) or more sodium chloride (NaCl) for growth. Most spe- (◀ Section 16.9). We begin our review of Euryarchaeota by reviewing cies of extreme halophiles require 2–4 M NaCl (12–23%) for the extremely halophilic Archaea. 4 UNIT T.D. Brock NASA (a) (b) Francisco Rodriguez-Valera Michael T. Madigan (c) (d) Figure 17.2 Hypersaline habitats for halophilic several times that of seawater. The green color is pri- A bloom of pigmented haloalkaliphiles is growing Archaea. Hypersaline habitats are home to the halo- marily from cells of cyanobacteria and green algae. in this pH 10 soda lake. Note the deposits of trona philic Archaea. These organisms not only tolerate salt (b) Aerial view near San Francisco Bay, California, of a (NaHCO3 # Na2CO3 # 2 H2O) around the edge of the lake. but require salt, and typically in large amounts. (a) The series of seawater evaporating ponds where solar salt (d) Scanning electron micrograph of halophilic bacte- north arm of Great Salt Lake, Utah, a hypersaline lake is prepared. The red-purple color is predominantly due ria including square Archaea present in a saltern in in which the ratio of ions is similar to that of seawater, to bacterioruberins and bacteriorhodopsin in cells of Spain. but in which absolute concentrations of ions are haloarchaea. (c) Lake Hamara, Wadi El Natroun, Egypt. M17_MADI4790_16_GE_C17.indd 594 04/03/2021 20:43  CHAPTER 17 Diversity of Archaea  595 optimal growth and can grow at salinities as high as 5.5 M NaCl Taxonomy and Physiology of Extremely (32%, the limit of saturation for NaCl), although some species grow Halophilic Archaea very slowly at this salinity. Some phylogenetic relatives of extremely The extremely halophilic Archaea are found within the taxonomic halophilic Archaea, for example species of Haloferax and Natronobac­ orders Halobacteriales, Natrialbales, and Haloferacales, which share a terium, are able to grow at much lower salinities, such as at or near common ancestor within the Euryarchaeota (Figure 17.1). These that of seawater (about 2.5% NaCl). three orders constitute the haloarchaea, but they are also sometimes called “halobacteria” because the genus Halobacterium (Figure 17.3), Hypersaline Environments: Chemistry and Productivity the best-studied representative of the extreme halophiles, was dis- Hypersaline habitats are common throughout the world, but covered and characterized long before the Archaea were recognized extremely hypersaline habitats are rare. Most such environments are as an independent domain. Many genera of Natrialbales, including in hot, dry areas of the world. Salt lakes can vary considerably in Natronobacterium, Natronomonas, and their relatives, differ from ionic composition. The predominant ions in a hypersaline lake other extreme halophiles in being extremely alkaliphilic as well as depend on the surrounding topography, geology, and general cli- halophilic. As befits the geochemistry of their soda lake habitat (Fig- matic conditions. Great Salt Lake in Utah (USA) (Figure 17.2a), for ure 17.2c), these natronobacteria grow optimally at low Mg2+ con- example, is essentially concentrated seawater. In this hypersaline lake centrations and alkaline pH (9–11). the relative proportions of the various ions [e.g., sodium (Na+), Haloarchaea stain gram-negatively, reproduce by binary fission, chloride (Cl-), and sulfate (SO42-)] are those of seawater, although and do not form spores. Cells of the various cultured genera are the overall concentration of ions is much higher. In addition, the rod-shaped, cocci, or cup-shaped, but even cells that form squares pH of this hypersaline lake is slightly alkaline. are known (Figure 17.2d). Cells of Haloquadratum are square and Soda lakes, in contrast, are highly alkaline hypersaline environ- only about 0.1 mm thick. Haloquadratum also forms gas vesicles ments. The water chemistry of soda lakes resembles that of hypersa- (◀ Section 2.7) that allow cells of this organism to float in its hyper- line lakes such as Great Salt Lake, but because high levels of saline habitat, probably as a means to be in contact with air since carbonate minerals are also present in the surrounding strata, the most extreme halophiles are obligate aerobes. Many other extremely pH of soda lakes is quite high. Waters of pH 10–12 are not uncom- halophilic Archaea also produce gas vesicles. A few strains of extreme mon in these environments (Figure 17.2c). In addition, the divalent 4 UNIT halophiles are weakly motile by archaella, the archaeal analog of bac- cations Ca2+ and Mg2+ are present in only trace amounts in soda terial flagella, that rotate to propel the cell forward (◀ Section 2.9), lakes because they precipitate out as carbonate salts at high pH and but most halophiles lack archaella. The genomes of Halobacterium carbonate concentrations. and Halococcus are unusual in that large plasmids (◀ Section 6.2) The diverse chemistries of hypersaline habitats have selected for containing up to 30% of the total cellular DNA are present and the a large diversity of halophilic microorganisms. Some organisms G + C base ratio of these plasmids (near 60% G + C) differs sig- are unique to one environment while others are widespread. nificantly from that of chromosomal DNA (66–68% G + C). Moreover, despite their extreme conditions, salt lakes can be highly productive ecosystems (the word productive here means high levels of autotrophic CO2 fixation). Archaea are not the only Nucleoids microorganisms present. The eukaryotic alga Dunaliella ( ▶ Figure 18.34a) is the major, if not the sole, oxygenic phototroph in most salt lakes. In highly alkaline soda lakes where Dunaliella is absent, anoxygenic phototrophic purple bacteria of the genera Ectothio­ Mary Reedy rhodospira and Halorhodospira ( ◀ Section 15.4) predominate. Organic matter originating from primary production by oxygenic or anoxygenic phototrophs sets the stage for growth of haloar- (a) chaea, which are chemoorganotrophic organisms. In addition, a few extremely halophilic chemoorganotrophic Bacteria, such as Halanaerobium, Halobacteroides, and Salinibacter, thrive in such environments. Marine salterns are also habitats for extreme halophiles. Marine salterns are enclosed basins filled with seawater left to evaporate, Mary Reedy eventually yielding solar sea salt (Figure 17.2b, d). As salterns approach the minimum salinity limits for haloarchaea, the waters turn a reddish-purple color due to the massive growth—called a (b) bloom—of cells (the red coloration apparent in Figure 17.2b and c is due to carotenoids and other pigments to be discussed later). Mor- Figure 17.3 Electron micrographs of thin sections of the extreme halophile phologically unusual Archaea are often present in salterns, including Halobacterium salinarum. A cell is about 0.8 mm in diameter. (a) Longitudinal section of a dividing cell showing the nucleoids. (b) High-magnification electron micrograph species with a square or cup-shaped morphology (Figure 17.2d). showing the glycoprotein subunit structure of the cell wall. Archaeal cell walls are Extreme halophiles are also present in highly salted foods, such as discussed in Section 2.5. certain types of sausages, marine fish, and salted pork. M17_MADI4790_16_GE_C17.indd 595 04/03/2021 20:43  596   UNIT 4 MICROBIAL DIVERSITY Plasmids from extreme halophiles are among the largest naturally Halophilic Cytoplasmic Components occurring plasmids known. Like cell wall proteins, cytoplasmic enzymes of Halobacterium are Most haloarchaea use amino acids or organic acids as electron highly acidic, but it is K+, not Na+, that is required for activity. This donors aerobically and require a number of growth factors such as makes sense because K+ is the predominant cation in the cytoplasm vitamins for optimal growth. A few haloarchaea oxidize carbohy- of cells of Halobacterium (Table 17.1). Besides having a highly acidic drates aerobically, but this capacity is rare; sugar fermentation does amino acid composition, halobacterial cytoplasmic proteins typi- not occur. Electron transport chains containing cytochromes of the cally contain lower levels of hydrophobic amino acids and lysine, a a, b, and c types are present in Halobacterium, and energy is con- positively charged (basic) amino acid, than do proteins of nonhal­ served via a proton motive force arising from electron transport ophiles. This is also to be expected because in a highly ionic cyto- (◀ Sections 3.8 and 3.9). Some haloarchaea can grow anaerobically, plasm, more polar proteins would tend to remain in solution as growth by anaerobic respiration linked to the reduction of nitrate whereas less polar proteins would tend to cluster and perhaps lose or fumarate (◀ Sections 3.10, 14.11, and 14.13) has been demon- activity. The ribosomes of Halobacterium also require high K+ levels strated in certain species. for stability, whereas ribosomes of nonhalophiles have no K+ requirement. Water Balance in Extreme Halophiles Extremely halophilic Archaea are thus well adapted to life in a Extremely halophilic Archaea require large amounts of NaCl for highly ionic environment. Cellular components exposed to the exter- growth. Detailed salinity studies of Halobacterium have shown that nal environment require high Na+ levels for stability, whereas cyto- the requirement for Na+ cannot be satisfied by any other ion, even plasmic components require high K+ levels. With the exception of a the chemically related ion potassium (K+). However, cells of Halo­ few extremely halophilic species of Bacteria that also use K+ as a bacterium need both Na+ and K+ for growth because each plays an compatible solute, in no other group of prokaryotic cells do we find important role in maintaining osmotic balance. this unique requirement for such high amounts of specific cations. As we learned in Section 4.15, microbes must withstand the osmotic forces they face in their habitats. To do so in a high-solute Bacteriorhodopsin and Light-Mediated ATP environment such as the salt-rich habitats of Halobacterium, organ- Synthesis in Haloarchaea 4 isms must either accumulate or synthesize solutes intracellularly. UNIT Certain species of haloarchaea can catalyze a light-driven synthesis These solutes are called compatible solutes (◀ Table 4.6). These of ATP. This form of phototrophy is not linked to CO2 fixation, and compounds counteract the tendency of the cell to become dehy- does not require chlorophyll pigments, and so it is not photosyn- drated under conditions of high osmotic strength by placing the thesis in the traditional sense. However, other light-sensitive pig- cell in positive water balance with its surroundings. Cells of Halo­ ments are present, including red and orange carotenoids—primarily bacterium, however, do not synthesize or accumulate organic com- C50 pigments called bacterioruberins—and inducible pigments pounds but instead pump large amounts of K+ from the involved in energy conservation; we discuss these pigments here. environment into the cytoplasm. This ensures that the concentra- Under conditions of low aeration, Halobacterium salinarum and tion of K+ inside the cell is even greater than the concentration of some other haloarchaea synthesize a protein called bacteriorhodopsin Na+ outside the cell (Table 17.1). This ionic condition maintains and insert it into their cytoplasmic membranes. Bacteriorhodopsin is positive water balance. so named because of its structural and functional similarity to rho- The Halobacterium cell wall (Figure 17.3b) is composed of glycopro- dopsin, the visual pigment of the eye. Conjugated to bacteriorhodop- tein and is stabilized by Na+. Sodium ions bind to the outer surface sin is a molecule of retinal, a carotenoid-like molecule that can absorb of the Halobacterium wall and are absolutely essential for maintaining light energy and pump a proton across the cytoplasmic membrane. cellular integrity. When insufficient Na+ is present, the cell wall breaks The retinal gives bacteriorhodopsin a purple hue. Thus cells of Halo­ apart and the cell lyses. This is a consequence of the exceptionally bacterium that are switched from growth under high-aeration condi- high content of the acidic (negatively charged) amino acids aspartate tions to O2-limiting growth conditions (a trigger of bacteriorhodopsin and glutamate in the glycoprotein of the Halobacterium cell wall. The synthesis) gradually change color from orange-red to purple-red negative charge on the carboxyl group of these amino acids is bound (Figure 17.2) as they synthesize bacteriorhodopsin and insert it into Mastering to Na+; when Na+ is diluted away, the negatively charged parts of the Microbiology their cytoplasmic membranes. Art Activity: proteins tend to repel each other, leading to cell lysis. Figure 17.4 Bacteriorhodopsin absorbs green light around 570 nm. Following Model for the absorption, the retinal of bacteriorhodopsin, which normally exists mechanism of bacteriorhodopsin in a trans configuration (RetT), becomes excited and converts to the TABLE 17.1 Concentration of ions in cells cis (RetC) form (Figure 17.4). This transformation is coupled to the of Halobacterium salinaruma translocation of a proton across the cytoplasmic membrane. The reti- nal molecule then decays to the trans isomer along with the uptake of Ion Concentration in medium (M) Concentration in cells (M) a proton from the cytoplasm, and this completes the cycle and resets Na + 4.0 1.4 the proton pump to repeat the process (Figure 17.4). As protons accu- K + 0.032 4.6 mulate on the outer surface of the membrane, a proton motive force Mg2+ 0.13 0.12 is generated that is coupled to ATP synthesis through the activity of a - proton-translocating ATPase (Figure 17.4; ◀ Section 3.9). Cl 4.0 3.6 a Data from Christian, J.H.B, and Waltho, J.A. 1962. Biochim. Biophys. Acta 65: 506. M17_MADI4790_16_GE_C17.indd 596 04/03/2021 20:43  CHAPTER 17 Diversity of Archaea  597 sense because levels of dissolved organic matter in the open oceans Out hp570nm In are typically very low, and thus a strictly chemoorganotrophic life- Cytoplasmic style would be difficult. membrane H+ H+ Check Your Understanding RetC RetT Why do cells of Halobacterium require high levels of Na+ for growth? Bacteriorhodopsin What benefit does bacteriorhodopsin confer on Halobacterium salinarum? H+ ATP H+ 17.2 Methanogenic Archaea H+ ADP + Pi KEY GENERA: Methanobacterium, Methanocaldococcus, ATPase Methanosarcina, Methanopyrus Many Euryarchaeota are methanogens, microorganisms that produce Figure 17.4 Model for the mechanism of bacteriorhodopsin. Light of 570 nm methane (CH4) as an integral part of their energy metabolism (hn570nm) converts the protonated retinal of bacteriorhodopsin from the trans form (methane production is called methanogenesis). In Section 14.15 we (RetT) to the cis form (RetC), along with translocation of a proton to the outer surface considered the unique biochemistry of methanogenesis. Later, we of the cytoplasmic membrane, thus establishing a proton motive force. ATPase will learn how methanogenesis is a major component of the global activity is driven by the proton motive force. carbon cycle, serving as the terminal step in the biodegradation of organic matter in many anoxic habitats ( ▶ Sections 21.1, 21.2, and Bacteriorhodopsin-mediated ATP production in H. salinarum sup- 21.9). Methanogens are important in a wide range of anoxic habitats ports slow growth of this organism under anoxic conditions. The including freshwater sediments, wetlands, rice paddies, wastewater light-stimulated proton pump of H. salinarum also functions to treatment plants, geothermal systems, the subsurface of the Earth’s 4 UNIT pump Na+ out of the cell by activity of a Na+ - H+ antiport system crust, and within the guts of many animals. and to drive the uptake of nutrients, including the K+ needed for osmotic balance. Amino acid uptake by H. salinarum is indirectly Diversity and Physiology of Methanogens driven by light as well, because amino acids are cotransported into Methanogens, often called by their nickname “methanoarchaea,” the cell with Na+ by an amino acid−Na+ symporter (◀ Section 2.2); occur in at least eight taxonomic orders, including Methanobacte­ removal of Na+ from the cell occurs by way of the light-driven riales, Methanococcales, Methanopyrales, Methanomassiliicoccales, Na+ - H+ antiporter. Methanomicrobiales, Methanocellales, Methanosarcinales, and Metha­ nonatronarchaeales (Figure 17.1). Methanogens exhibit consider- Other Rhodopsins able morphological and physiological diversity (Figure 17.5 and see Besides bacteriorhodopsin, at least three other rhodopsins are present Table 17.2). As can be seen in Figure 17.1, methanogens are wide- in the cytoplasmic membrane of cells of H. salinarum. Halorhodopsin spread within the Euryarchaeota and do not represent a single is a light-driven chloride (Cl-) pump that brings Cl- into the cell as coherent phylogenetic group. We have already been introduced to the anion for K+. The retinal of halorhodopsin binds Cl- and trans- the factors that cause inconsistency between phylogenetic diversity ports it into the cell. Two other light sensors, called sensory rhodopsins, and functional diversity (◀ Section 15.1). In the case of methano- are present in H. salinarum. These light sensors control phototaxis genesis it is most likely that the ability to reduce CO2 to CH4 (movement toward light, ◀ Section 2.12) by the organism. Through evolved only once within the Euryarchaeota, and that gene loss the interaction of a cascade of proteins similar to those in chemotaxis caused lineages such as the haloarchaea and Thermoplasmatales to (◀ Sections 2.11 and 7.6), sensory rhodopsins affect archaellar rota- lose the capacity to produce methane. We will also see that Archaeo­ tion, moving cells of H. salinarum toward light where bacteriorho- globus (Section 17.4) still retains some of the genes encoding methan­ dopsin can function to make ATP (Figure 17.4). ogenesis and can actually produce methane under certain growth We will learn when we consider marine microbiology ( ▶ Sections conditions. 20.11 and 20.12) that diverse species of chemoorganotrophic Bacteria Methanogens have diverse physiological characteristics, but they that inhabit the upper layers of the ocean contain bacteriorhodopsin- are united by their ability to produce methane and by their intoler- like proteins called proteorhodopsins. As far as is known, proteorho- ance to O2. Several cofactors required by methanogenic pathways dopsin functions like bacteriorhodopsin except that different are inhibited by O2, and hence all methanogens are obligate anaer- spectral forms exist, each form being tuned to the absorption of its obes. As a result, strict anoxic techniques are necessary for their own specific wavelength of light. Although the energy generated cultivation in isolation. While most methanogens are mesophilic from proteorhodopsin alone is insufficient to sustain growth, these and do not live in extreme environments, a diversity of species marine bacteria use proteorhodopsin as a supplement to the ATP have been described including some that grow optimally at very they generate from respiration. Proteorhodopsin as a mechanism high (see Figure 17.7) or very low temperatures, at very high salt for energy conservation in marine bacteria makes good ecological concentrations, or at extremes of pH. M17_MADI4790_16_GE_C17.indd 597 04/03/2021 20:43  598   UNIT 4 MICROBIAL DIVERSITY Alexander Zehnder Alexander Zehnder Alexander Zehnder Alexander Zehnder (a) (b) (c) (d) Figure 17.5 Scanning electron micrographs of cells of diverse species of methanogenic Archaea. (a) Methanobrevibacter ruminantium. A cell is about 0.7 mm in diameter. (b) Methanobrevibacter arboriphilus. A cell is about 1 mm in diameter. (c) Methanospirillum hungatei. A cell is about 0.4 mm in diameter. (d) Methanosarcina barkeri. A cell is about 1.7 mm wide. Methanogens possess a diversity of cell envelope and cell wall fermentative anaerobes (◀ Section 14.22, ▶ Section 21.2). In these configurations. Methanobacterium species and relatives (Figure 17.6a) cooperative systems, the fermentative organisms degrade a wide have cell walls composed of pseudomurein (◀ Section 2.3). Methano­ range of organic molecules into H2, CO2, and acetate, which are sarcina and relatives (Figure 17.6b) have cell walls composed of ultimately used as substrates for methanogenesis. methanochondroitin (so named because of its structural resemblance The three methanogenic pathways are distributed across different to chondroitin, the connective tissue polymer of vertebrate ani- phylogenetic groups of methanogens (Table 17.3). Methanogenesis mals). In addition, Methanocaldococcus (Figure 17.7a) and Methano­ by CO2 reduction occurs widely across the known diversity of meth- planus species have cell walls composed of protein or glycoprotein, anogens, but not all methanogens can reduce CO2. Notably, many respectively. Finally, species such as Methanospirillum (Figure 17.5c) species of Methanosarcinales, and all species in the Methanomassili­ 4 UNIT use an S-layer (◀ Section 2.5) as their cell wall. icoccales, Methanonatronarchaeales, and the genus Methanosphaera have lost the ability to produce methane by CO2 reduction (Table Methanogenic Pathways 17.3). The CO2 reduction pathway also allows some methanogens Methanogenesis occurs through three different pathways (Table 17.2): to produce methane from formate or carbon monoxide. In addition, CO2 reduction (◀ Figure 14.38), methylotrophic methanogenesis while H2 is the typical electron donor for methanogenesis by (◀ Figure 14.39a), and acetoclastic methanogenesis (◀ Figure CO2 reduction, this pathway also allows some methanogens to 14.39b). Each of these pathways relies on coenzyme M; methane is reduce CO2 by using electrons from pyruvate or certain alcohols ultimately produced by reduction of methyl-CoM to methane (Tables 17.2 and 17.3). (◀ Section 14.15). Through these pathways, methanogens convert Acetoclastic methanogenesis is performed by few methanogens a limited number of substrates into methane (Table 17.2). Interest- and is found exclusively within the Methanosarcinales (Table 17.3). ingly, these substrates do not include such common compounds as Methanogenesis from acetate is a dominant source of methane pro- glucose, organic acids (other than pyruvate), or fatty acids (other duction in a wide range of environments ( ▶ Section 21.2). In ace- than acetate). Methanogens often form syntrophic associations with toclastic methanogenesis, electron flow is branched, producing both J.G. Zeikus and V.G. Bowen J.G. Zeikus and V.G. Bowen (a) (b) Figure 17.6 Transmission electron micrographs of thin sections of methanogenic Archaea. (a) Methanobrevibacter ruminantium. A cell is 0.7 mm in diameter. (b) Methanosarcina barkeri, showing the thick cell wall and the manner of cell segmentation and cross-wall formation. A cell is 1.7 mm in diameter. M17_MADI4790_16_GE_C17.indd 598 04/03/2021 20:43  CHAPTER 17 Diversity of Archaea  599 Helmut König and K.O. Stetter R. Rachel and K.O. Stetter (a) (b) König/Stetter Stephen Zinder (c) (d) Figure 17.7 Hyperthermophilic and thermophilic methanogens. (a) Methanocaldococcus jannaschii (temperature optimum, 858C), 4 UNIT shadowed preparation electron micrograph. A cell is about 1 mm in diameter. (b) Methanotorris igneus (temperature optimum, 888C), thin section. A cell is about 1 mm in diameter. (c) Methanothermus fervidus (temperature optimum, 888C), thin-sectioned electron micrograph. A cell is about 0.4 mm in diameter. (d) Methanosaeta thermophila (temperature optimum, 608C), phase-contrast micrograph. A cell is about 1 mm in diameter. The refractile bodies inside the cells are gas vesicles. CO2 and CH4 as products. Acetoclastic methanogens perform a dismu- in important ways. Some methylotrophic methanogens use a tation of acetate in which the carboxyl group is oxidized to CO2 while branched pathway that produces both CH4 and CO2 as products the methyl group is reduced to CH4 (Table 17.2, ◀ Figure 14.39b). and allows for carbon assimilation from methylated compounds. The reductive acetyl-CoA pathway is then used to assimilate carbon Other methylotrophic methanogens use a methyl-reducing pathway into cell biomass. that produces only CH4 as a product and does not allow for carbon Methylotrophic methanogenesis can take many forms, but all assimilation from methylated compounds. The branched pathway methylotrophic methanogens use one of two pathways that differ is found only within the family Methanosarcinales. Branched path- ways for methylotrophic methanogenesis are similar conceptually to the acetoclastic pathway with a major difference being that meth- TABLE 17.2 The three methanogenic pathways ylotrophs do not perform a dismutation, instead oxidizing one and their substrates molecule to CO2 so that they can reduce other molecules to CH4 (Table 17.2). For example, many species of Methanosarcinales oxi- I. CO2 reduction pathway: electrons are typically derived from H2 dize one molecule of CH3OH to CO2 to generate the six electrons Carbon dioxide, CO2 Formate, HCOO- needed to reduce three molecules of CH3OH to 3 CH4 and 3 H2O Carbon monoxide, CO (◀ Figure 14.39a). In addition, methylotrophic methanogens that II. Acetoclastic pathway: electrons are derived from dismutationa use a branched pathway funnel carbon from their oxidative branch Acetate, CH3COO- into the reductive acetyl-CoA pathway in order to assimilate carbon Pyruvate, CH3COCOO- from methylated compounds. III. Methylotrophic pathways: electrons are derived either by oxidizing The methyl-reducing pathway for methylotrophic methanogenesis, some of the methylated substrate to CO2 (branched pathway) or in contrast, does not result in the production of CO2, and methano- by the oxidation of H2 or formate (methyl-reducing pathway) Methanol, CH3OH gens using the methyl-reducing pathway lack the ability to assimilate Methylamine, CH3NH3+ carbon from methylated compounds. Methylotrophic methanogens Dimethylamine, (CH3)2NH2+ such as Methanosphaera stadtmanae are unable to oxidize methyl Trimethylamine, (CH3)3NH+ groups to CO2 and therefore require an external electron donor— Methyl mercaptan, CH3SH Dimethyl sulfide, (CH3)2S either H2 or formate—to reduce the methyl group to methane (Tables 17.2 and 17.3). Hence, M. stadtmanae produces CH4 but not CO2 a In a dismutation, one part of the molecule is reduced by oxidizing another part of the same molecule. M17_MADI4790_16_GE_C17.indd 599 04/03/2021 20:43  600   UNIT 4 MICROBIAL DIVERSITY Methanocaldococcus jannaschii as a Model Methanogen TABLE 17.3 Characteristics of some methanogenic The genomes of the hyperthermophilic methanogen Methanocaldo­ Archaeaa coccus jannaschii (Figure 17.7a) and many other methanogens have Substrates for been sequenced. The 1.66-megabase-pair (Mbp) circular genome of Order/Genus Pathwaysb methanogenesisc M. jannaschii, an organism that has been used as a model for the Methanomicrobiales I molecular study of methanogenesis and archaeal motility, contains Methanomicrobium I about 1700 genes, and genes encoding enzymes of methanogenesis H2 + CO2, formate and several other key cell functions have been identified. Interest- Methanospirillum I H2 + CO2, formate ingly, the majority of M. jannaschii genes encoding functions such Methanoculleus I H2 + CO2, formate, as central metabolic pathways and cell division are similar to those alcohols + CO2 in Bacteria. By contrast, most of the M. jannaschii genes encoding Methanococcales I core molecular processes such as transcription and translation more Methanococcus I H2 + CO2, formate, closely resemble those of eukaryotes. These findings reflect the vari- pyruvate + CO2 ous traits shared by organisms in the three cellular domains and are Methanocaldococcus I H2 + CO2 consistent with our understanding of how the three domains of cells Methanopyrales I evolved, as discussed in Chapter 13. However, analyses of the Methanopyrus I H2 + CO2 M. jannaschii genome also show that fully 40% of its genes have no Methanocellales I counterparts in genes from either of the other domains. Some of Methanocella I H2 + CO2 these are genes that encode the enzymes needed for methanogene- sis, of course, but many others likely encode novel cellular functions Methanobacteriales I, III absent from cells in the other domains or may encode redundant Methanobacterium I H2 + CO2, formate functions carried out by classes of enzymes distinct from those Methanobrevibacter I H2 + CO2, formate found in Bacteria and Eukarya. Methanothermus I H2 + CO2 4 Methanopyrus, a Hyperthermophilic Methanogen UNIT Methanothermobacter I H2 + CO2, formate, CO Methanosphaera III H2 + methanol Methanopyrus (Figure 17.8), the only genus in the order Methanopy­ Methanosarcinales I, II, III rales, is a rod-shaped hyperthermophilic methanogen that shares Methanosarcina I, II, III H2 + CO2, methanol, phenotypic properties with both the hyperthermophiles (see Section methylamines, acetate, CO 17.12) and the methanogens. Methanopyrus was isolated from hot Methanococcoides III Methanol, methylamines sediments near submarine hydrothermal vents and from the walls of “black smoker” hydrothermal vent chimneys (Section 17.11; Methanohalophilus III Methanol, methylamines, methyl sulfides ▶ Section 20.16 and Figure 20.46). Methanopyrus produces CH4 only Methanosaeta II Acetate from H2 + CO2 and grows rapidly for an autotrophic organism Methanosalsum III Methanol, methylamines, dimethyl sulfide R. Rachel and K.O. Stetter Methanimicrococcus III H2 + 1 methanol, methylamines 2 Methanomassiliicoccales III Methanomassiliicoccus III H2 + methanol Methanomethylophilus III H2 + methanol Methanonatronarcheales III (a) Methanonatronarchaeum III H2 + 1 methanol, methylamines, dimethyl sulfide2 CH3 O a  Taxonomic orders are listed in bold. An order is a taxonomic rank that consists of several families; CH3 CH3 CH3 CH3 families consist of several genera (◀ Table 13.1). b Methanogenic pathways I–III are summarized in Table 17.2. CH3 c  Methylamines can include the substrates methylamine (CH3NH3+), dimethylamine ((CH3)2NH2+ ), and O trimethylamine ((CH3)3NH + ); methyl sulfides can include dimethyl sulfide ((CH3)2S) and methyl mer- CH3 CH3 CH3 CH3 captan (CH3SH). OH Ether linkage (b) from methylated substrates. In addition, although M. stadtmanae and metabolically similar methanogens can make methane from methyl- Figure 17.8 Methanopyrus. Methanopyrus grows optimally at 1008C and can make ated compounds, they are unable to incorporate them as a carbon CH4 only from CO2 + H2. (a) Electron micrograph of a cell of Methanopyrus kandleri, the most thermophilic of all known organisms (upper temperature limit, 1228C). This cell source. Instead, they typically require an organic carbon source such measures 0.5 * 8 mm. (b) Structure of the novel lipid of M. kandleri. This is the normal as acetate, though a few species can also fix CO2. Besides M. stadtma­ glycerol diether of Archaea (◀ Figure 2.3b) except that the side chains are an unsatu- nae, this pattern of methylotrophic methanogenesis is also character- rated form of phytanyl (called geranylgeraniol) rather than phytanyl. istic of Methanomicrococcus blatticola and species in the orders Methanomassiliicoccales and Methanonatronarchaeales (Table 17.3). M17_MADI4790_16_GE_C17.indd 600 04/03/2021 20:43  CHAPTER 17 Diversity of Archaea  601 (generation time ,1 h at 1008C). In special pressurized vessels, growth of one strain of Methanopyrus has been recorded at 1228C, the highest temperature yet shown to support microbial growth (Sections 17.12 and 17.13). In addition to its remarkable tolerance to high temperature, Meth­ anopyrus is also unusual because it contains membrane lipids found in no other known organism. Recall that in the lipids of Archaea, the glycerol side chains contain phytanyl rather than fatty acids bonded in ether linkage to the glycerol (◀ Section 2.1 and Figure 2.3a). In Methanopyrus, this ether-linked lipid is an unsaturated form of the otherwise saturated biphytanyl tetraethers found in all other hyper- thermophilic Archaea (Figure 17.8b). These unusual lipids are thought to help stabilize the cytoplasmic membrane of Methanopyrus T.D. Brock at its unusually high growth temperatures. Some Euryarchaeota lack cell walls and we consider them next. (a) Check Your Understanding What are the three major pathways of methanogenesis and in what phylogenetic groups are they found? What physiological and structural features distinguish the Methanosarcinales from other methanogens? 17.3 Thermoplasmatales 4 UNIT KEY GENERA: Thermoplasma, Picrophilus, Ferroplasma A phylogenetically distinct line of Archaea contains thermophilic and extremely acidophilic genera: Thermoplasma, Ferroplasma, and Picrophilus. These organisms are among the most acidophilic of all A. Segerer and K.O. Stetter known microbes, with Picrophilus being capable of growth even below pH 0. Most are thermophilic as well. These genera also form their own taxonomic order within the Euryarchaeota, the Thermoplas­ matales (Figure 17.1). We begin with a description of the mycoplasma- like organisms Thermoplasma and Ferroplasma. (b) Archaea Lacking Cell Walls Figure 17.9 Thermoplasma species. (a) Thermoplasma acidophilum, an acido­ Thermoplasma and Ferroplasma lack cell walls, and in this respect they philic and thermophilic mycoplasma-like archaeon; electron micrograph of a thin resemble the mycoplasmas (◀ Section 16.9). Thermoplasma section. The diameter of cells varies from 0.2 to 5 mm. The cell shown is about 1 mm (Figure 17.9) is a chemoorganotroph that grows optimally at 558C in diameter. (b) Shadowed preparation of cells of Thermoplasma volcanium isolated and pH 2 in complex media. Two species of Thermoplasma have been from hot springs. Cells are 1–2 mm in diameter. Notice the abundant ar­chaella (the described, Thermoplasma acidophilum and Thermoplasma volcanium. rotating structures that confer swimming motility on Archaea, ◀ Section 2.9) and Species of Thermoplasma are facultative aerobes, growing either aero- irregular cell morphology. bically or anaerobically by sulfur respiration (◀ Section 14.12). Most strains of T. acidophilum have been obtained from self-heating material called lipoglycan. This substance consists of glycolipids con- coal refuse piles. Coal refuse contains coal fragments, pyrite (FeS2), taining sugars such as mannose and glucose (Figure 17.11), and these and other organic materials extracted from coal. When dumped into glycolipids form a tetraether lipid monolayer membrane. The hydro- piles in surface mining operations, coal refuse heats as a result of phobic core of this glycolipid consists of biphytanyl (◀ Section 2.1 microbial metabolism bringing it to combustion temperature and Figure 2.3b). In Thermoplasma and similar organisms such as (Figure 17.10). This sets the stage for growth of Thermoplasma, which Sulfolobus, this basic biphytanyl structure can be modified to include likely metabolizes organic compounds leached from the hot coal one to four cyclopentane rings, with the number of rings tending to refuse. The second species, T. volcanium, has been isolated in hot increase in proportion to the temperature of the environment. These acidic soils throughout the world and is highly motile by multiple glycolipids constitute a major fraction of the total lipids of Thermo­ archaella (Figure 17.9b). plasma. The membrane also contains glycoproteins and glycophos- To survive the osmotic stresses of life without a cell wall and to pholipids, but not sterols. These molecules render the Thermoplasma withstand the dual environmental extremes of low pH and high membrane stable to hot, acidic conditions. temperature, Thermoplasma has evolved a unique cytoplasmic mem- Like mycoplasmas (◀ Section 16.9), Thermoplasma contains a rela- brane structure. The membrane contains a lipopolysaccharide-like tively small genome (1.5 Mbp). In addition, Thermoplasma DNA is M17_MADI4790_16_GE_C17.indd 601 04/03/2021 20:43  602   UNIT 4 MICROBIAL DIVERSITY Picrophilus A phylogenetic relative of Thermoplasma and Ferroplasma is Picrophi­ lus. Although Thermoplasma and Ferroplasma are extreme acidophiles, Picrophilus is even more so, growing optimally at pH 0.7 and capable of growth at pH values lower than 0. Picrophilus also has a cell wall (an S-layer; ◀ Section 2.5, Figures 2.14 and 2.36a) and a much lower DNA G + C base ratio than does Thermoplasma or Ferroplasma. Although phylogenetically related, Thermoplasma, Ferroplasma, and Picrophilus have quite distinct genomes. Two species of Picrophilus have been isolated from acidic Japanese solfataras, and like Thermo­ T.D. Brock plasma, both grow heterotrophically on complex media. The physiology of Picrophilus is of interest as a model for extreme acid tolerance. Studies of its cytoplasmic membrane point to an Figure 17.10 A typical self-heating coal refuse pile, habitat of Thermoplasma. unusual arrangement of lipids that forms a highly acid-impermeable The pile, containing coal debris, pyrite, and other microbial substrates, self-heats membrane at very low pH. By contrast, at moderate acidities such as a result of microbial metabolism. as pH 4, the membranes of cells of Picrophilus become leaky and disintegrate. Obviously, this organism has evolved to survive only complexed with a highly basic DNA-binding protein that organizes in highly acidic habitats and shows the most extraordinary the DNA into globular particles resembling the nucleosomes of acidophily of any known microbe. eukaryotic cells. This protein is homologous to the histone-like DNA-binding protein HU of Bacteria, which plays an important role Check Your Understanding in organization of the DNA in the cell. In contrast, several other In what ways are Thermoplasma and Picrophilus similar? Euryarchaeota contain basic proteins homologous to the DNA- In what ways do they differ? binding histone proteins of eukaryotic cells. How does Thermoplasma strengthen its cytoplasmic 4 UNIT membrane to survive without a cell wall? Ferroplasma Ferroplasma is a chemolithotrophic relative of Thermoplasma. Ferro­ plasma is a strong acidophile; however, it is not a thermophile, as it 17.4 Thermococcales and Archaeoglobales grows optimally at 358C. Ferroplasma oxidizes ferrous iron (Fe2 + ) to ferric iron (Fe3 + ) to obtain energy and uses CO2 as its carbon source. KEY GENERA: Thermococcus, Pyrococcus, Archaeoglobus, The oxidation of Fe2 + results in acidification of the environment. Ferroglobus Ferroplasma grows in mine tailings containing pyrite, which is its A few euryarchaeotes thrive in thermal environments and some are energy source. The extraordinary acidophily of Ferroplasma allows it hyperthermophiles. We consider here the Thermococcales and to drive the pH of its habitat down to extremely acidic values. After Archaeoglobales, which are two orders of Euryarchaeota that contain moderate acidity is generated from Fe2 + oxidation by acidophilic hyperthermophilic species (Figure 17.1). organisms such as Acidithiobacillus ferrooxidans and Leptospirillum fer­ rooxidans ( ▶ Sections 21.6, 22.1, and 22.2), Ferroplasma becomes Thermococcus and Pyrococcus active and subsequently generates the very low pH values typical of Thermococcus and Pyrococcus are genera within the order Thermococ­ acid mine drainage. Acidic waters at pH 0 can be generated by the cales. Thermococcus is a spherical hyperthermophilic euryarchaeote activities of Ferroplasma. indigenous to anoxic thermal waters in various locations through- out the world. The spherical cells contain a tuft of polar archaella and are thus highly motile (Figure 17.12a). Thermococcus is an obli- Ether linkage HO gately anaerobic chemoorganotroph that metabolizes proteins and O O other complex organic mixtures (including some sugars) with O elemental sulfur (S0) as electron acceptor at temperatures from 55 O to 958C. [R] Glu (c1 1) O Pyrococcus (Figure 17.12b) is morphologically similar to Thermo­ coccus. Pyrococcus differs from Thermococcus primarily by its higher R = Man (c1 2) Man (c1 4) Man (c1 3) temperature requirements; Pyrococcus grows between 70 and 1068C with an optimum of 1008C. Thermococcus and Pyrococcus are also Figure 17.11 Structure of a tetraether glycolipid of Thermoplasma acidophilum. The dominant glycolipids of T. acidophilum have two polar head groups that are connected metabolically quite similar. Proteins, starch, or maltose are oxidized by ether linkages to a hydrophobic core. This structure causes them to form a thermo- as electron donors, and S0 is the terminal electron acceptor and is stable lipid monolayer (◀ Figure 2.3b). One or both of the polar head groups typically reduced to hydrogen sulfide (H2S). Both Thermococcus and Pyrococ­ contains a mono- or oligosaccharide that contains glucose (Glu), mannose (Man), cus form H2S when S0 is present, but form H2 when S0 is absent (see and other sugars. The hydrophobic core consists of the straight-chain caldarchaeol Table 17.4). (shown), which can be modified to include one to four cyclopentane rings (not shown). M17_MADI4790_16_GE_C17.indd 602 04/03/2021 20:43  CHAPTER 17 Diversity of Archaea  603 Archaeoglobus was a methanogen that lost many of the genes required for methanogenesis. Furthermore, genome analysis suggests that the ancestor of Archaeoglobus acquired genes for sulfate reduction as a result of horizontal gene transfer from sulfate-reducing bacteria within the Deltaproteobacteria (◀ Section 15.11). Ferroglobus (Figure 17.13b) is related to Archaeoglobus but is not a sulfate reducer. Instead, Ferroglobus is an iron-oxidizing chemo­ H. König and K.O. Stetter G. Fiala and K.O. Stetter lithotroph, conserving energy from the oxidation of Fe2 + to Fe3 + coupled to the reduction of nitrate (NO3-) to nitrite (NO2-) (see Table 17.4). Ferroglobus grows autotrophically and can also use H2 or H2S as electron donor in its energy metabolism. Ferroglobus was isolated from a shallow marine hydrothermal vent and grows opti- (a) (b) mally at 858C. Figure 17.12 Spherical hyperthermophilic Euryarchaeota from submarine vol­ Ferroglobus is interesting for several reasons, but especially for its canic areas. (a) Thermococcus celer; electron micrograph of shadowed cells (note ability to oxidize Fe2 + to Fe3 + under anoxic conditions. This process tuft of archaella). (b) Dividing cell of Pyrococcus furiosus; electron micrograph of might help explain the origin of some Fe3 + found in ancient rocks thin section. Cells of both organisms are about 0.8 mm in diameter. dated to before the predicted appearance of cyanobacteria on Earth (◀ Section 13.2). With organisms like Ferroglobus, it would have been Archaeoglobus and Ferroglobus possible for Fe2 + oxidation to proceed without the need for O2 as an electron acceptor. The metabolism of Ferroglobus thus has implica- Archaeoglobus was isolated from hot marine sediments near hydro- tions for dating the origin of cyanobacteria and the subsequent oxy- thermal vents. In its metabolism, Archaeoglobus couples the oxida- genation of Earth. Certain anoxygenic phototrophic bacteria can also tion of H2, lactate, pyruvate, glucose, or complex organic compounds oxidize Fe2 + under anoxic conditions (◀ Section 14.8), and so sev- to the reduction of SO42 - to H2S. Cells of Archaeoglobus are irregular