Advertisement

The Family Ferroplasmaceae

  • Olga V. Golyshina
Reference work entry

Abstract

The family Ferroplasmaceae (Golyshina et al. Int J Syst Evol Microbiol 50:997–1006, 2000) is represented by cell wall-lacking, acidophilic, facultatively anaerobic, mesophilic or moderately thermophilic, and iron-metabolizing archaea. Phylogenetic relatives are members of families Thermoplasmaceae and Picrophilaceae. Presently, the family Ferroplasmaceae embraces the genera Ferroplasma and Acidiplasma. The genus Ferroplasma is monospecific considering only one member with a validly published name, Ferroplasma acidiphilum (Golyshina et al. Int J Syst Evol Microbiol 50:997–1006, 2000); the genus Acidiplasma includes two species, named A. cupricumulans (Golyshina et al. Int J Syst Evol Microbiol 59:2815–2823, 2009), initially described as Ferroplasma cupricumulans (Hawkes et al. Extremophiles 10:525–530, 2006, Int J Syst Evol Microbiol 58:1–2, 2008), and A. aeolicum (Golyshina et al. Int J Syst Evol Microbiol 59:2815–2823, 2009). Members of the family exhibit some differences in their physiological and chemotaxonomic properties and populate acidic, iron/sulfidic environments worldwide.

Keywords

Type Strain Mineral Salt Medium Trace Element Solution Mineral Salt Medium Medium Pregnant Leachate Solution 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Taxonomy, Historical and Current

Short Description of the Family and Their Genera

Ferroplasmaceae Golyshina et al. 2000

Fer.ro.plas.ma’ce.ae. M.L. Gr. neut. n. Ferroplasma type genus of the family; ferro pertaining to ferrous iron; plasma something shaped or molded; L. -aceae ending denoting a family; M.L. Ferroplasmaceae a family of ferrous iron-oxidizing forms (modified from Golyshina et al. 2000).

Phylogenetically the family is a member of the order Thermoplasmatales (Huber and Stetter 2006) within the kingdom Euryarchaeota within the domain Archaea. The nearest phylogenetic neighbors occupy families Thermoplasmaceae and Picrophilaceae.

The family contains type genus Ferroplasma (Golyshina et al. 2000; emended by Pivovarova et al. 2002 and by Dopson et al. 2004) and genus Acidiplasma (Golyshina et al. 2009). The phylogenetic distance between two genera is about 95.4 % 16S rRNA gene sequence similarity.

The members are characterized by the lack of cell wall and morphologically represented by pleomorphic, spherical, and irregular cocci forms. Nonmotile. Obligate acidophilic with optima for growth varying from 1.0 to 1.7. Aerobic to facultative anaerobic. Mesophilic or moderate thermophilic. Capable of chemomixotrophic, chemoautotrophic, and chemoorganotrophic growth.

General properties of two type strains of these genera are represented in Table 5.1.
Table 5.1

Selected general characteristics of Ferroplasma acidiphilum, YT, and Acidiplasma aeolicum, VT

Character

Ferroplasma acidiphilum YT

Acidiplasma aeolicum VT

Morphology

Polymorphic, irregular cocci Length 1.0–3.0/width 0.3–1.0 μm

Spherical (0.5–1 μm), irregular cocci, or filamentous Length 0.5–3/width 0.2–0.5 μm

Range for growth

pH

1.3–2.2

0–4

T °C

15–45

15–65

Chemoorganotrophy

±a

+

Facultative anaerobic

±a

+

Fe2+ oxidation

+

+

Main sugar components in its major dibiphytanyl phosphoglycerol lipids

β-Glucose

β-Galactose

DNA G + C content (mol%)

36.5

36

aConflicting results

The main polar lipids are glycosyl/galactosyl dibiphytanyl phosphoglycerol tetraethers. The predominant respiratory lipoquinones are naphthoquinones.

Phylogenetic Structure of the Family and Its Genera

The family Ferroplasmaceae was established to include the genus Ferroplasma by Golyshina and co-workers (2000), based on the SSU rRNA gene-based phylogenetic position of the genus Ferroplasma and distinguishing characteristics from the members of families Thermoplasmaceae and Picrophilaceae. The genus Acidiplasma was added to the family by Golyshina and colleagues (2009) on the basis of its phylogenetic position (Fig. 5.1). Based upon 16S rRNA gene sequence analysis, the family Ferroplasmaceae is more related to the family Picrophilaceae with the genus Ferroplasma being the most distant. The genus Acidiplasma forms a tight monophyletic cluster on 16S rRNA gene sequences from strains VT, BH2T, JTC3, and L1 exhibiting higher optimal (or growth range) temperatures, in comparison to more mesophilic data for the strains of the genus Ferroplasma.
Fig. 5.1

Phylogenetic reconstruction of the family Ferroplasmaceae based on 16S rRNA and created using the maximum likelihood algorithm RAxML (Stamatakis 2006). The sequence datasets and alignments were used according to the All-Species Living Tree Project (LTP) database (Yarza et al. 2010). Representative sequences from closely related taxa were used as out-groups. In addition, a 40 % maximum frequency filter was applied in order to remove hypervariable positions and potentially misplaced bases from the alignment. Scale bar indicates estimated sequence divergence

Molecular Analyses

DNA-DNA hybridization (DDH) studies have been performed for the type strain of Ferroplasma acidiphilum DSM 12658T and other strains with 99.6–99.7 % 16S rRNA gene sequence identities with the type strain. DDH values (from 72.8 ± 5.5 to 91.3 ± 3.1) revealed close relatedness between the tested strains, suggesting, according to the recommendations of Wayne and co-workers (1987), that they represent the same species. Ferroplasma acidiphilum DSM 12658T and the strain fer1, referred as representing a different species, “F. acidarmanus,” had the DDH similarity of 71.7 ± 7.0 % (Dopson et al. 2004) being 100 % identical on the level of 16S rRNA gene sequence.

DDH analysis has been done for two type strains of the genus Acidiplasma, Acidiplasma aeolicum DSM 18409T and Acidiplasma cupricumulans DSM 16551T that have 100 % identical 16S rRNA gene sequences showed 46.4 and 53.1 % DNA-DNA reassociation values in two independent measurements (Golyshina et al. 2009). Discrimination by DDH of Acidiplasma cupricumulans BH2T and “Ferroplasma thermophilum” strain L1 (the latter name is so far not validated) identified the value 46.3 % with 99 % identity in their 16S rRNA gene sequences (Zhou et al. 2008). After all necessary additional proceedings for the validation, therefore, the strain L1 could be transferred to the genus Acidiplasma.

Pulsed-field gel electrophoresis of chromosomal DNA of strains Ferroplasma acidiphilum YT and F. acidiphilum Y-2 has been performed by Pivovarova and colleagues (2002). Protein profiling analyses have also been conducted for the investigation of phylogenetic relationships between the family members (Pivovarova et al. 2002). The proteome studies for the members of the family have been mostly used for the physiological and functional characterizations (Ferrer et al. 2005; Dopson et al. 2005; Golyshina et al. 2006; Ferrer et al. 2007; Potrykus et al. 2011).

Another molecular approach, the amplified ribosomal DNA restriction enzyme analysis (ARDREA) (Johnson et al. 2005), has been used for the identification of the members of the family in acidophilic microbial communities.

No studies on riboprinting or ribotyping have so far been conducted for the members of the family.

Genome Analysis

No complete genome sequence data for the type strains of the family has been published up to date. The only genome data available is the draft genome (gapped sequence) of the strain fer1, “Ferroplasma acidarmanus” (Allen et al. 2007).

Viruses

No viruses and plasmids harboring the type strains of the family are known up to date.

Phenotypic Analysis

Ferroplasma Golyshina et al. 2000, Updated Descriptions of Pivovarova et al. 2002; Dopson et al. 2004

Ferroplasma (Fer.ro.plasma. M.L. ferro pertaining to ferrous iron; Gr. neut. n. plasma something shaped or molded; M.L. Ferroplasma a ferrous-iron-oxidizing form).

Cells are irregular cocci, polymorphic, with the size in length 1.0–3.0 μm and in width from 0.3 μm to 1.0 μm, and could be spherical or filamentous, in duplex and triplex forms, nonmotile (Fig. 5.2).
Fig. 5.2

Electron image of a thin section of Ferroplasma acidiphilum. Bar 500 nm (The micrograph was kindly provided by Dr. Heinrich Lünsdorf, HZI, Braunschweig)

Gram negative. Cell wall and S-layer are absent. Comparative analysis of total lipids revealed that about 90 % of total lipids are represented by two types of glycophospholipids: beta-d-glucopyranosylcaldarchaetidylglycerol (about 55 %—lipid 1) and trihexosylcaldarchaetidylglycerol (26 %—lipid II). The hydrolysate of carbohydrate fraction of lipid I contained only d-glucose, and the lipid II hydrolysate contained both d-glucose and d-galactose in a proportion of 2:1 (Pivovarova et al. 2002; Batrakov et al. 2002).

The genus contains a single species with a validly published name, the type strain, Ferroplasma acidiphilum YT, DSM 12658T. There are other isolates within the genus Ferroplasma, similar on 16S rRNA sequence with invalidly published names up to date.

The type strain Ferroplasma acidiphilum YT is characterized by next features. Acidophilic: pH range for the growth is 1.3–2.2 with the optimum pH 1.7. Mesophilic, the growth range is 15–45 °C with the optimum at 35 °C. Aerobic. Chemoautotrophic. Oxidizes Fe2+ to Fe3+ from FeSO4 and pyrite in the presence of low concentrations of the yeast extract (0.02 %) supposed to be used as a growth factor. Concentrations of yeast extract higher than 0.2 % were inhibiting for growth, and growth only on yeast extract in the absence of iron has not been detected (Golyshina et al. 2000).

Dopson et al. (2004) suggested the ability for the type strain to chemoorganotrophic (measured to be as extremely weak indeed), to chemomixotrophic, and, possibly, to chemoautotrophic growth. Also a weak anaerobic growth at the expense of Fe(III) reduction in cultures containing ferric iron and 0.02 % of yeast extract in long-term experiments (22 days) has been observed, and the type strain was therefore suggested to be a facultative anaerobe (Dopson et al. 2004).

The source of the isolation of the type strain is a bioleaching reactor produced during oxidation of an arsenogold/arsenopyrite concentrate from the Bakyrchikskoe ore deposit (Kazakhstan).

G + C content is 36.5 mol%.

Acidiplasma Golyshina et al. 2009

(A.ci.di.plasma. N.L. neut. n acidum an acid; Gr. neut. n. plasma something shaped or molded; N.L. neut. n. Acidiplasma an acid-living form).

Cells are irregular cocci, spherical (0.5–1 μm), or filamentous, with the size in length 0.5–3 μm and in width from 0.2 μm to 0.5 μm, nonmotile. Cell wall and S-layer are absent.

Principal membrane lipids are represented by dibiphytanyl phosphoglycerol tetraether compounds varying in the number of cyclopentyl rings (0–4).

The polar lipids are composed by galactosyl dibiphytanyl phosphoglycerol tetraether. Minor fraction is represented by mono- and diglycosyl dibiphytanyl ether lipids and the corresponding phosphoglycerol derivatives. The predominant respiratory lipoquinones are known to be naphthoquinones.

The mol G + C of DNA is 34–36 %.

The type species is Acidiplasma aeolicum (Golyshina et al. 2009). The type strain is VT.

The genus contains two species, named Acidiplasma aeolicum (Golyshina et al. 2009) and Acidiplasma cupricumulans previously described as Ferroplasma cupricumulans (Hawkes 2008; Golyshina et al. 2009).

The two type strains show 100 % of 16S rRNA gene sequence identity; on the basis of DDH analysis results, however, they belong to different species (Golyshina et al. 2009). Both type strains are facultative anaerobic, moderately thermophilic, acidophilic, and iron-metabolizing organisms.

In addition, Acidiplasma aeolicum has the following characteristics: pH range for the growth is 0–4.0 with the optimum pH 1.4–1.6. Moderately thermophilic, the range of temperatures for growth is 15–65 °C with the optimum at 45 °C. Oxidizes Fe2+ from FeSO4 in the presence of low concentrations of yeast extract (0.02 %), supposed to be a growth factor. Chemoorganotrophic growth is observed on the yeast extract or on a mixture of yeast extract and glucose as substrates. Other organic substrates are not used. Anaerobic growth is detected in yeast extract medium and in the medium with ferric iron, supplemented with tetrathionate and low amounts of yeast extract (Golyshina et al. 2009).

Source: hydrothermal pool on Vulcano Island, Italy.

Acidiplasma cupricumulans is characterized by these features: pH range for the growth is 0.4–1.8 with the optimum pH 1.0–1.2. The range of temperatures for growth is 22–63 °C with the optimum at 54 °C. Not able to chemoorganotrophic growth (Hawkes et al. 2006, 2008).

Source: bioleaching reactor containing sulfide ore from Monywa, Myanmar. The type strain is BH2T.

Isolation, Enrichment, and Maintenance Procedures

Isolation and Enrichment

Ferroplasma acidiphilum YT was isolated by the method of serial dilution from enrichments established with the liquid phase taken from a bioreactor operating with a gold-containing arsenopyritic ore concentrate from Bakyrchik (Kazakhstan). The medium used for isolation was modified medium 9 K (Silverman and Lundgren 1959), which has in a content (g L−1) MgSO4 × 7H2O 0.4, (NH4)2SO4 0.2, KCl 0.1, K2HPO4 0.1, and FeSO4 × 7H2O 25, supplemented with trace element solution (Segerer and Stetter 1992a) and 0.02 % of yeast extract. A solution of FeSO4 × 7H2O was sterilized separately in a small volume (45 mL of H2O and 5 mL of 10 % H2SO4) and added to a basal salt solution after sterilization. The pH (ca. 1.7) of the medium was adjusted by 10 % H2SO4. The cultivation of the strain was managed at 35 °C with shaking for 5–7 days (Golyshina et al. 2000).

Alternatively another medium (MSM) containing the salts (in g L−1) (NH4)2SO4, 3.0; Na2SO4 × 10H2O, 3.2; KCl, 0.1; K2HPO4, 0.05; MgSO4 × 7H2O, 0.5; and Ca(NO3)2, 0.01, could be used for growth. Mineral salt medium (MSM) is supplemented by yeast extract, 0.02 %; filter sterilized solution of FeSO4, 20 g L−1; and trace element solution (Dopson et al. 2004). Solid media could be prepared using double-concentrated MSM medium with abovementioned supplements and solidified with agarose of Sigma Type I/BRL Ultrapure at a final concentration of 0.5 %. Incubations at 37 °C yielded growth after 3 weeks—small, round, and white colonies were obtained, but authors noticed very low plating efficiency. Cultivation on solid medium with an “overlay technique” described by Johnson and Hallberg (2007) could be used for the isolation of acidophilic iron-oxidizing archaea as Ferroplasma acidiphilum.

Acidiplasma aeolicum strain VT was isolated from an enrichment culture established with a volcanic sand/gravel sample (5 % w/v) taken from hydrothermal pool from Vulcano Island, Italy, in medium 9 K prepared, cultivated, and isolated in a pure culture, in a similar manner as it was specified for Ferroplasma acidiphilum, strain YT with some modifications: these included adjusting the medium to pH 1.5 and supplementing the medium 9 K with K2S4O6 (5 mM), which was filter sterilized and added to the medium after sterilization (Golyshina et al. 2009). Acidiplasma aeolicum strain VT grows organotrophically in the modified medium AB (Segerer et al. 1988) supplemented with yeast extract and glucose (0.1 %, w/v for each). More specifically, the medium AB contained the following salts (g L−1): (NH4)2SO4 1.3, KH2PO4 0.28, MgSO4 × 7H2O 0.25, and CaCl2 × 2H2O 0.07, supplemented with trace element solution (Segerer and Stetter 1992a). The cultivation of Acidiplasma aeolicum strain VT is managed at 45 °C with shaking (Golyshina et al. 2009). Anaerobic growth was observed in 100 mL volume closed vessels with medium 9 K containing ferric sulfate and supplemented with 0.02 % (w/v) yeast extract and potassium tetrathionate (5 mM) as the electron donor and in the modified medium AB (Segerer et al. 1988) supplemented with yeast extract (0.1 %, w/v) and glucose (0.1–1 %). Both media (9 K and AB) were flushed with pure N2 and a mixture of N2/CO2 (80:20, vol/vol, with the same gas mixtures in the headspace (Golyshina et al. 2009).

Acidiplasma cupricumulans strain BH2T was isolated from enrichment culture established with a pregnant leachate solution, collected from Myanmar Ivanhoe Copper Company heaps, and inoculated into the medium containing (g L−1) (NH4)2SO4, 1.5; MgSO4 × 7H2O, 0.25; KH2PO4, 0.25; and yeast extract, 0.1, supplemented with FeSO4, 10, and Na2S2O4, 2, and statically incubated at 50 °C. The medium pH was adjusted to 1.8 with concentrated H2SO4. The isolation of the strain Acidiplasma cupricumulans BH2T has been proceeded by the method of serial decimal dilution to extinction on the same medium, used for the establishment of the enrichment, adjusted to pH 0.8 (Hawkes et al. 2006).

The growth of strains of Ferroplasmaceae could be maintained in different volume glass bottles or in fermentors.

Maintenance

Members of the family could be preserved for a short time (1–2 months) at room temperature and remain viable. Cryopreservation is possible with 20 % glycerol solution or 5 % DMSO in growth media at −70 °C, but a preliminary 10–100-fold concentration of cultures before cryopreservation is recommended, and longer-term cryopreserved cultures are preferentially stored in liquid nitrogen.

Ecology

Ore deposits and hydrothermal pool located in volcanic zones are ecosystems from where the type strains of the family were isolated. Numerous documentations on clones attributed to the Ferroplasmaceae, and recent metagenomic surveys revealed a wide geographical distribution and ubiquity of the members of this family. Specific habitats of Ferroplasmaceae are represented by different types of acidic ecosystems which could be sulfidic iron- and metal-containing mines, ore deposits, heaps, acid mine drainage streams, or their natural equivalents as Rio Tinto, natural areas known to be inhabited by acidophiles, e.g., as the sites with geothermal activity or cave systems with favorable microenvironments (summarized by Golyshina (2011)). Search for Ferroplasmaceae in volcanic areas in the Eastern Hemisphere alone revealed the presence of these archaea on Vulcano Island (Italy), Nisyros Island (Greece), and Sao Miguel Island of Azores (Portugal), (Figs. 5.3, 5.4, 5.5, and 5.6). Being important contributors to the global iron and sulfur cycling, Ferroplasmaceae attract significant attention for the reason of environmental acid generation and biotechnological relevance.
Fig. 5.3

Fragment of hydrothermal pool on Vulcano Island (Italy)

Fig. 5.4

Vulcano Island (Italy) with visible solfataric areas

Fig. 5.5

The pool on Sao Miguel Island (Azores, Portugal)

Fig. 5.6

Solfataric areas on the Nisyros Island (Greece)

Pathogenicity and Clinical Significance

No data about pathogenicity of type strains of Ferroplasmaceae is known.

Application

Biomining

Iron-oxidizing acidophilic prokaryotes including the type strains of Ferroplasmaceae have been known for some decades for their contribution to the processes of dissolution of sulfide minerals. Biomining capabilities of these microorganisms, especially those of the family Ferroplasmaceae, have been well documented in a number of studies (Pivovarova et al. 2002; Okibe et al. 2003; Hawkes et al. 2006; Remonsellez et al. 2009; Zhou et al. 2008; and others).

Enzymes

A range of acidophilic enzymes from type strain Ferroplasma acidiphilum YT have been cloned and expressed in E. coli. These include DNA ligase, three alpha-glycosidases, and a carboxylesterase. These enzymes showed unusually low pH optima in vitro, iron dependence, and a number of diverse and potentially applicable features (Ferrer et al. 2005, 2008; Golyshina et al. 2006).

References

  1. Allen EE, Tyson GW, Whitaker RJ, Detter JC, Richardson PM, Banfield JF (2007) Genome dynamics in a natural archaeal population. Proc Natl Acad Sci USA 104:1883–1888PubMedCentralPubMedCrossRefGoogle Scholar
  2. Batrakov SG, Pivovarova TA, Esipov SE, Sheichenko VI, Karavaiko GI (2002) Beta-d-glucopyranosyl caldarchaetidylglycerol is the main lipid of the acidophilic, mesophilic, ferrous iron-oxidising archaeon Ferroplasma acidiphilum. Biochim Biophys Acta 1581:29–35PubMedCrossRefGoogle Scholar
  3. Dopson M, Baker-Austin C, Hind A, Bowman JP, Bond PL (2004) Characterization of Ferroplasma isolates and Ferroplasma acidarmanus sp. nov., extreme acidophiles from acid mine drainage and industrial bioleaching environments. Appl Environ Microbiol 70:2079–2088PubMedCentralPubMedCrossRefGoogle Scholar
  4. Dopson M, Baker-Austin C, Bond PL (2005) Analysis of differential protein expression during growth states of Ferroplasma strains and insights into electron transport for iron oxidation. Microbiology 151:4127–4137PubMedCrossRefGoogle Scholar
  5. Ferrer M, Golyshina OV, Plou FJ, Timmis KN, Golyshin PN (2005) A novel alpha-glucosidase from the acidophilic archaeon Ferroplasma acidiphilum strain Y with high transglycosylation activity and an unusual catalytic nucleophile. Biochem J 391:269–276PubMedCentralPubMedCrossRefGoogle Scholar
  6. Ferrer M, Golyshina OV, Beloqui A, Golyshin PN, Timmis KN (2007) The cellular machinery of Ferroplasma acidiphilum is iron-protein-dominated. Nature 445:91–94PubMedCrossRefGoogle Scholar
  7. Ferrer M, Golyshina OV, Beloqui A, Böttger LH, Andreu JM, Polaina J, De Lacey AL, Trautwein AX, Timmis KN, Golyshin PN (2008) A purple acidophilic di-ferric DNA ligase from Ferroplasma. Proc Natl Acad Sci USA 105:8878–8883PubMedCentralPubMedCrossRefGoogle Scholar
  8. Golyshina OV (2011) Environmental, biogeographic, and biochemical patterns of archaea of the family Ferroplasmaceae. Appl Environ Microbiol 77:5071–5078PubMedCentralPubMedCrossRefGoogle Scholar
  9. Golyshina OV, Pivovarova TA, Karavaiko GI, Kondratéva TF, Moore ER, Abraham WR, Lünsdorf H, Timmis KN, Yakimov MM, Golyshin PN (2000) Ferroplasma acidiphilum gen. nov. sp. nov., an acidophilic, autotrophic, ferrous-iron-oxidizing, cell-wall-lacking, mesophilic member of the Ferroplasmaceae fam. nov., comprising a distinct lineage of the Archaea. Int J Syst Evol Microbiol 50:997–1006PubMedCrossRefGoogle Scholar
  10. Golyshina OV, Golyshin PN, Timmis KN, Ferrer M (2006) The “pH optimum anomaly” of intracellular enzymes of Ferroplasma acidiphilum. Environ Microbiol 8:416–425PubMedCrossRefGoogle Scholar
  11. Golyshina OV, Yakimov MM, Lünsdorf H, Ferrer M, Nimtz M, Timmis KN, Wray V, Tindall BJ, Golyshin PN (2009) Acidiplasma aeolicum gen. nov. sp. nov., a novel euryarchaeon of the family Ferroplasmaceae isolated from a hydrothermal pool, and transfer of Ferroplasma cupricumulans to Acidiplasma cupricumulans comb. nov. Int J Syst Evol Microbiol 59:2815–2823PubMedCrossRefGoogle Scholar
  12. Hawkes RB, Franzmann PD, O’Hara G, Plumb JJ (2006) Ferroplasma cupricumulans sp. nov., a novel moderately thermophilic, acidophilic archaeon isolated from an industrial-scale chalcocite bioleach heap. Extremophiles 10:525–530PubMedCrossRefGoogle Scholar
  13. Hawkes RB, Franzmann PD, O’Hara G, Plumb JJ (2008) Ferroplasma cupricumulans sp. nov. in list of new names and new combinations previously effectively, but not validly, published, validation list no. 119. Int J Syst Evol Microbiol 58:1–2CrossRefGoogle Scholar
  14. Huber H, Stetter KO (2006) The order Thermoplasmatales. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds) The prokaryotes—a handbook on the biology of bacteria, vol 3, 3rd edn. Springer, New York, pp 101–112Google Scholar
  15. Johnson DB, Hallberg KB (2007) Techniques for detecting and identifying acidophilic mineral-oxidizing microorganisms. In: Rawlings DE, Johnson DB (eds) Biomining. Springer, Berlin/Heidelberg, pp 237–261CrossRefGoogle Scholar
  16. Johnson DB, Okibe N, Hallberg KB (2005) Differentiation and identification of iron-oxidizing acidophilic bacteria using cultivation techniques and amplified ribosomal DNA restriction enzyme analysis. J Microbiol Methods 60:299–313PubMedCrossRefGoogle Scholar
  17. Okibe N, Gericke M, Hallberg KB, Johnson DB (2003) Enumeration and characterization of acidophilic microorganisms isolated from a pilot plant stirred tank bioleaching operation. Appl Environ Microbiol 69:1936–1943PubMedCentralPubMedCrossRefGoogle Scholar
  18. Pivovarova TA, Kondrat’eva TF, Batrakov SG, Esipov SE, Sheichenko VI, Bykova SA, Lysenko AM, Karavaiko GI (2002) Phenotypic features of Ferroplasma acidiphilum strains YT and Y-2. Microbiology (Msk) 71:809–818Google Scholar
  19. Potrykus J, Jonna VR, Dopson M (2011) Iron homeostasis and responses to iron limitation in extreme acidophiles from the Ferroplasma genus. Proteomics 11:52–63PubMedCrossRefGoogle Scholar
  20. Remonsellez F, Galleguillos F, Moreno-Paz M, Parro V, Acosta M, Demergasso C (2009) Dynamic of active microorganisms inhabiting a bioleaching industrial heap of low-grade copper sulfide ore monitored by real-time PCR and oligonucleotide prokaryotic acidophile microarray. Microb Biotechnol 2:613–624PubMedCentralPubMedCrossRefGoogle Scholar
  21. Segerer AH, Stetter KO (1992) The genus Thermoplasma. In: Balows A, Truper HG, Dvorkin M, Harder W, Schleifer K-H (eds) The prokaryotes, 2nd edn. Springer, New York, pp 684–701Google Scholar
  22. Segerer A, Langworthy TA, Stetter KO (1988) Thermoplasma acidophilum and Thermoplasma volcanium sp. nov. from solfatara fields. Syst Appl Microbiol 10:161–171CrossRefGoogle Scholar
  23. Silverman MP, Lundgren DG (1959) Studies on the chemoautotrophic iron bacterium Ferrobacillus ferrooxidans. 1: an improved medium and harvesting procedure for securing high cell yields. J Bacteriol 77:642–647PubMedCentralPubMedGoogle Scholar
  24. Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690PubMedCrossRefGoogle Scholar
  25. Wayne LG, Brenner DJ, Colwell RR, Grimont PAD, Kandler O, Krichevsky MI, Moore LH, Moore WEC, Murray RGE et al (1987) International committee on systematic bacteriology. Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int J Syst Bacteriol 37:463–464CrossRefGoogle Scholar
  26. Yarza P et al (2010) Update of the all-species living tree project based on 16S and 23S rRNA sequence analyses. Syst Appl Microbiol 33:291–299, http://www.arb-silva.de/projects/living-tree
  27. Zhou H, Zhang R, Hu P, Zeng W, Xie Y, Wu C, Qiu G (2008) Isolation and characterization of Ferroplasma thermophilum sp. nov., a novel extremely acidophilic, moderately thermophilic archaeon and its role in bioleaching of chalcopyrite. J Appl Microbiol 105:591–601PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  1. 1.School of Biological SciencesBangor UniversityBangorUK

Personalised recommendations