Biotechnological applications derived from microorganisms of the Atacama Desert

Review ArticleBiotechnological Applications Derived from Microorganisms ofthe Atacama Desert

Armando Azua-Bustos1 and Carlos Gonzaacutelez-Silva2

1 Blue Marble Space Institute of Science Seattle WA 98109 USA2Centro de Investigacion del Medio Ambiente (CENIMA) Universidad Arturo Prat 1110939 Iquique Chile

Correspondence should be addressed to Armando Azua-Bustos ajazuauccl

Received 7 April 2014 Revised 29 June 2014 Accepted 7 July 2014 Published 23 July 2014

Academic Editor Ameur Cherif

Copyright copy 2014 A Azua-Bustos and C Gonzalez-Silva This is an open access article distributed under the Creative CommonsAttribution License which permits unrestricted use distribution and reproduction in any medium provided the original work isproperly cited

The Atacama Desert in Chile is well known for being the driest and oldest desert on Earth For these same reasons it is alsoconsidered a good analog model of the planet Mars Only a few decades ago it was thought that this was a sterile place but inthe past years fascinating adaptations have been reported in the members of the three domains of life low water availability highUV radiation high salinity and other environmental stresses However the biotechnological applications derived from the basicunderstanding and characterization of these species with the notable exception of copper bioleaching are still in its infancy thusoffering an immense potential for future development

1 Introduction

The Atacama Desert located in northern Chile betweenlatitudes 17∘ and 27∘ south has average annual rains of lessthan 2mm [1] In comparison other known deserts in theworld like the Mojave Desert in North America [2] or theSahara Desert in Africa [3] have average annual rains of116mm and 100mm respectively These extremely low rainrates have determined the Atacama Desert to be classified asa hyperarid desert [4] (a desert with an aridity index of lessthan 005 as the evapotranspiration of water from its soils ismuch higher than the inputs of rains)The Atacama Desert isalso unique as it is believed to be the oldest desert on Earthbeing arid for the last 150 million years and hyperarid for thepast 15 million years [5 6]

Thus the Atacama has been an extremely dry desertfor a very long time and only forty years ago it wasthought that nothing could live in its seemingly barrenlandscapes (Figure 1(a)) However during the past ten yearsculture dependent and independent methods have unveileda plethora of microorganisms (Bacteria Archaea andEukarya) that were able to adapt and evolve in very specificand unexpected habitats of this desert [7] Habitats as diverse

as the underside of quartz rocks [8] fumaroles at the AndesMountains [9] the inside of halite evaporites [10] and cavesof the Coastal Range [11 12] showed that microbial life foundnovel ways to adapt to the extreme conditions typical ofthe Atacama extremely low water availability intense solarradiation and high salinity (for a more complete descriptionof Atacamarsquos microbial species please see our recent reviewon this subject [7]) However up to date very few works havegone beyond the descriptive stage of establishing what typesof microorganisms may be found in specific microenviron-ments [13] thus explaining the incipient biotechnologicalapplications derived from knowledge that still being gained

The study of the molecular strategies used by microbiallife in other extreme environments (high temperature forexample) gave rise tomany biotechnological applications thatare now of standard use [14] In a similar way the characteri-zation of the molecular strategies evolved bymicroorganismsof the Atacama to cope with its exceptional abiotic stresses(desiccation in particular) should be multiple and uniqueand thus novel sources of metabolites and genes for thebiotechnological industry In this review the few reportedcases of the biotechnological use of AtacamaDesert microor-ganisms to date are summarized

Hindawi Publishing CorporationBioMed Research InternationalVolume 2014 Article ID 909312 7 pageshttpdxdoiorg1011552014909312

2 BioMed Research International

(a) (b)

(c)

Figure 1 Examples of habitats of the Atacama Desert from where biotechnological applications have been derived or used (a) The centralvalley the hyperarid core of the Atacama Desert (b) Heap bioleaching at Radomiro Tomic an open pit copper mine owned by the ChileanCopper Corporation (Codelco) Note the copper rich blue-green solution obtained from the heaps (c) The Loa River a typical arsenic richriver of the Atacama Desert Image credits Panels A and C Armando Azua-Bustos Panel B Armando Azua Aroz

2 Applications Derived from Members ofthe Bacteria Domain

Copper Bioleaching Copper bioleaching or ldquobiominingrdquoallowed the usage of insoluble copper sulphides and oxidesthrough hydrometallurgy as opposed to the traditionaltechnology of pyrometallurgy Compared to pyrometallurgybioleaching has the advantage of being a simpler processrequiring less energy and equipments (Figure 1(b)) In addi-tion bioleaching does not produce sulfur dioxide emissionsan important factor for the Chilean mining towns whichwere usually built alongside the extracting operations inChile (most of which are located in the Atacama Desert)Bioleaching also offered a better treatment of low grade(again the usual case in Atacama copper ores) or wasteores and in many cases it is the only way to treat themLow-grade ores (06 and less) are abundant in Chilebut their processing by pyrometallurgy in most cases isnot economical Through bioleaching copper was able tobe extracted from ore minerals like chalcopyrite (CuFeS2)with the crucial contribution of chemolithotrophic microbialspecies extremely tolerant to low pH which use the reducedsulphur as an energy source The most known of thesemicroorganisms is Acidithiobacillus ferrooxidans [15] butother species like Leptospirillum ferrooxidans Sulfobacillusacidophilus and Acidimicrobium ferrooxidans are thought toalso participate in the bioleaching process [16 17]

In Chile the first mine that introduced bioleaching wasSociedad Minera Pudahuel (a copper mine not located inthe Atacama) in the 1980s Today this process is extensivelyused in the Chilean copper mining industry [18 19] reachingover 16 million tons of copper per year [19] It has beenestimated that Chilersquos copper actual reserves would increaseup to 50 if all copper sulphides could be economicallytreated by bioleaching [19]

Acidithiobacillus ferrooxidans has been identified in dif-ferent places of the Atacama Desert [20 21] Some of thesespecies have been found in sulfidic mine tailings dumps inthe marine shore at Chanaral Bay [21] located at the CoastalRange of the Atacama This is of particular interest as thesespecies were found to be halotolerant iron oxidizers activeat NaCl concentrations up to 1M in enrichment culturesHigh concentrations of chloride ions inhibit the growth of theacidophilic microorganisms traditionally used in biomining[22] Thus the finding of halotolerant bioleaching specieswould allow the use of seawater for biomining operations inthe future a very important advancement in a region wherewater availability has always been extremely low

Bioleaching strains found in the Atacama Desert havebeen recently patented as is the case of Acidithiobacillus fer-rooxidans strainWenelenDSM 16786 [23] andAcidithiobacil-lus thiooxidans strain Licanantay DSM 17318 [24] (US Patentnumbers 7601530 and 7700343) Both strains showedimproved oxidizing activity when compared to standard

BioMed Research International 3

strains isolated elsewhere like Acidithiobacillus ferrooxidansATCC 23270 and Acidithiobacillus thiooxidans ATCC 8085StrainWenelen an iron and sulfur oxidizing microorganismwas particularly efficient in oxidizing chalcopyrite whilestrain Licanantay a strict sulfur oxidizer showed activityin both primary and secondary sulfured minerals suchas chalcopyrite covellite bornite chalcocite enargite andtennantite [24ndash26]

Recently the comparative genomic analysis and me-tabolomic profiles of these two strains were obtained whichturned helpful for determining basic aspects of its regulatorypathways and functional networks biofilm formation energycontrol and detoxification responses [27 28]

As for Archaea although some species have beenreported in acid mine drainage in the Atacama [21] there areyet no reports of strains specifically isolated for industrial use

Biomedicine Soils of the Atacama shelter a numberof bacterial species with promising characteristics for thebiomedical industry One of the first descriptions of microor-ganisms that are known to produce such biomolecules waspublished in 1966 by Cameron et al [29] Commissioned byNASA this group approached the Atacama as a way to obtainbasic information on terrestrial desert environments and itsmicrobiota in order to develop and test the instruments to betaken to Mars ten years later by the Viking Mission Amongothers they were among the first to report the presenceof Streptomyces species Bacillus subtilis aterrimus Bacillusbrevis Bacillus cereus andMicrococcus caseolyticus howeverno details of biomolecules produced by these species werelater reported

Almost forty years passed until a groundbreaking reportby McKayrsquos group in 2003 [30] showed that when the experi-ments performed by theViking landers on the surface ofMarswere repeated with soils of the Yungay region of the AtacamaDesert the same results were obtained essentially This leadsto the recognition of the Atacama Desert as one of the driestplaces on Earth causing then a surge of reports focusing onthe characteristics of variousmicroenvironmental conditionsin the Atacama and its related microbiology [7]

Later on the interest in the potential biomedical use ofthese recently reported species started focusing on speciesof the Actinobacteria as these were previously known assynthesizers of useful molecules [31] Among this latter classspecies like Amycolatopsis Lechevalieria and Streptomyceshave been reported at various arid and hyperarid sites of theAtacama [32]

Members of the Streptomycetes are a well-known sourceof antibiotics [33] and Lechevalieria species are known tohave nonribosomal peptide synthase (NRPS) gene clustersthat synthesize antitumoral compounds [31] Accordinglyof the species found by Okororsquos group [32] all of theAmycolatopsis and Lechevalieria andmost of the Streptomycesisolates tested positive for the presence of NRPS genes Thissame group determined later the metabolic profile of oneof these Streptomyces strains (strain C34) identifying threenew compounds from the macrolactone polyketides class[34] and other compounds like deferoxamine E hygromycinA and 510158401015840-dihydrohygromycin These compounds showeda strong activity against the Gram-positive bacteria tested

(Staphylococcus aureus Listeria monocytogenes and Bacillussubtilis) but weak activity against the tested Gram-negativebacteria (E coli and Vibrio parahaemolyticus)

In a parallel report they also found that strain C34synthetized four new antibiotics of the ansamycin-typepolyketides with antibacterial activity against both Staphy-lococcus aureus ATCC 25923 and Escherichia coli ATCC25922 [35] In particular chaxamycin D4 showed a selectiveantibacterial activity against S aureus ATCC 25923 Anotherof these strains Streptomyces sp C38 synthetized three newmacrolactone antibiotics (atacamycins AndashC) which exhibitedmoderate inhibitory activity against the enzyme phospho-diesterase (PDE-4B2) [36] Inhibitors of PDE (the mostfamous of this group being Viagra) can prolong or enhancethe effects of physiological responses mediated by cAMPand cGMP by inhibition of their degradation by PDE andare considered potential therapeutics for pulmonary arterialhypertension coronary heart disease dementia depressionand schizophrenia [37] In the case of atacamycin A it alsoshowed anti proliferative activity against cell lines of coloncancer (CXF DiFi) breast cancer (MAXF 401NL) uteruscancer (UXF 1138L) and colon RKO cells [36]

Similar positive results were obtained by Leiros et al 2014[38] in which seven molecules synthetized by Streptomycessp Lt 005 Atacama Streptomyces C1 and Streptomyces spCBS 19865 were tested against hydrogen peroxide stress inprimary cortical neurons as potentially new drugs for theavoidance of neurodegenerative disorders such as Parkin-sonrsquos and Alzheimerrsquos diseases The reported compoundsinhibited neuronal cytotoxicity and reduced reactive oxygenspecies (ROS) release after 12 h of treatment Among thesecompounds the quinone anhydroexfoliamycin and the redpyrrole-type pigment undecylprodigiosin showed the bestprotection against oxidative stress with mitochondrial func-tion improvement ROS production inhibition and increaseof antioxidant enzymes like glutathione and catalase In addi-tion both compounds showed a modest caspase-3 activityinduced by the apoptotic enhancer staurosporine

In a different work another group of secondary metabo-lites called abenquines were found to be synthetized byStreptomyces sp Strain DB634 isolated from the soils ofthe Altiplano of the Atacama [39] These abenquines (AndashD)showed modest inhibitory activity against Bacillus subtilisdermatophytic fungi phosphodiesterase type 4b and antifi-broblast proliferation (NIH-3T3)

An interesting case to discuss in this section of a commer-cially successful but controversial example of a compoundproduced from an Actinobacteria isolated from anotherwell-known Chilean environment is that of rapamycin (alsoknown as sirolimus) isolated by Brazilian researchers froma strain of Streptomyces hygroscopicus endemic of EasternIsland or Rapa Nui [40] Rapamycin was originally usedas an antibiotic but later on it was discovered to showpotent immunosuppressive and antiproliferative properties[41 42] and even claimed to extend life span [43] Sadlynothing of this development benefited the Chilean economyas agreements like the United Nations Rio Declaration onEnvironment and Development were yet to be established


Arsenic Bioremediation Conventional arsenic removal indrinking water such as reverse osmosis and nanofiltration areeffective and able to remove up to 95 of the initial arsenicconcentrations but the operating costs of these plants arehigh [44] In addition the oxidation of As (III) to As (V) is aprerequisite for all conventional treatment processes and asthis is an extremely slow reaction toxic and costly oxidantssuch as chlorine hydrogen peroxide or ozone must be usedas catalysts [44 45] Thus an attractive alternative solutionfor arsenic removal is bioremediation as a wide variety ofbacteria can use it as an electron donor for autotrophicgrowth or as an electron acceptor for anaerobic respiration[46ndash48]

In the case of theAtacamaDesert the first steps leading tothe biosequestration of arsenic by endemic microorganismsare nowbeing takenThis toxicmetalloid is naturally found inrivers of the Atacama Desert (Figure 1(b)) as arsenate As (V)and the most toxic species arsenite As (III) [49ndash51] Amongother negative biological effects arsenate being a chemicalanalog of phosphate inhibits oxidative phosphorylation andarsenite binds to sulfhydryl groups of proteins [52] It isprecisely in the sediments of one of these rivers (Camaronesriver near the coastal city of Arica) with arsenic concentra-tion in water (1100 120583g Lminus1) and sediments (550 120583g Lminus1) that49 isolates were identified and distributed between the 120572-Proteobacteria (5 isolates) 120573-Proteobacteria (13 isolates) and120574-Proteobacteria (26 isolates) [44 53] Most of these speciesbelonged to the genera Alcaligenes Burkholderia Coma-monas Enterobacter Erwinia Moraxella Pantoea SerratiaSphingomonas and Pseudomonas [53] of which AlcaligenesBurkholderia Sphingomonas Pantoea Erwinia and Serratiawere not previously reported in literature as arsenic tolerantFittingly eleven of the arsenic-tolerant isolates had the genears that codes for the critical enzyme involved in this reactionarsenate reductase [53] In a later work from this groupit was found that one of the species isolated Pseudomonasarsenicoxydans strain VC-1 was able to tolerate up to 5mMof As (III) being also capable of oxidizing at high rates thetotality of the arsenite present in themedium with lactate as acarbon source [54]Thus the characterization of these speciesin experimental bioreactors will certainly offer interestingoptions for future water and soil bioremediation [55]

3 Applications Derived from MicrobialMembers of the Eukarya Domain

BiomedicineCarotenoids are lipid soluble tetraterpenoid pig-ments synthesized as hydrocarbons (carotene eg lycopene120572-carotene and 120573-carotene) or their oxygenated derivatives(xanthophylls eg lutein 120572-cryptoxanthin zeaxanthin etc)by microorganisms and plants [56] In these organismsthey play multiple and critical roles in photosynthesisby maintaining the structure and function of photosyn-thetic complexes contributing to light harvesting quenchingchlorophyll triplet states scavenging reactive oxygen speciesand dissipating excess energy [57 58] Up to date more than700 carotenoids have been described [59] Yellow orangeand red carotenoids are used as pharmaceuticals animal feed

additives and colorants in cosmetics and foods Interest indietary carotenoids has increased in the past years due to theirantioxidant and anti-inflammatory potential [60 61] as theyare very efficient quenchers of singlet oxygen and scavengersof other reactive oxygen species [62] Carotenoids are alsoimportant precursors of retinol (vitamin A) [62 63]

Among other sources species of the halophilic biflag-ellate unicellular green alga Dunaliella (Chlorophyta) likeDunaliella salina are industrially cultivated as a naturalsource of beta-carotene around the world including Chile[64] Under conditions of abiotic stress (high salinity hightemperature high light intensity and nitrogen limitation) upto 12 of the algal dry weight is 120573-carotene [65 66] whichaccumulates in oil globules in the interthylakoid spaces oftheir chloroplast [65] In addition as a defense mechanismagainst hypersalinity D salina synthetizes high amounts ofthe compatible solute glycerol anothermolecule of economicvalue [67]

There are several species of the genusDunaliella reportedin theAtacamaDesertmainly in hypersaline lagoons [68 69]and even growing aerophytically on cave walls [11] In thecase of D Salina Isolate Conc-007 isolated from the Salar deAtacama it was found to be capable of synthesizing 100 pgof beta-carotene per cell two to four times higher thanother species used in commercial beta-carotene production[69 70] In turn D salina SA32007 also isolated from theSalar de Atacama synthesized triglycerides-enriched lipidsunder nitrogen deficiency conditions a potentially relevantresult for biodiesel production [71] Important differencesin the carotenogenic capacity of the D salina strains havebeen shown to be dependent on the high genetic diversityof member of this species [69] This is highly relevant forthe case of the Chilean species as it seems that they maybe better producers of 120573-carotene and other biomolecules incomparison to other species of the world

An additional factor to consider in this case is thatDunaliella production facilities elsewhere (Australia Chinaand India) are located in areas where solar irradiance ismaximal climate is warm and hypersaline water is available[57] which are precisely the characteristics of most areas ofthe Atacama thus growth facilities may well be developedin this desert using endemic strains In addition adaptivelaboratory evolution [72] and metabolic engineering may beapplied to theAtacama species in the future as thesemethodshave recently been investigated and accomplished [72 73]

4 Final Comments

Thebrevity of this review reflects how little has been advancedto date in the biotechnological use of members of themicrobial world found in the Atacama Desert This may beunderstood Although the Atacama is well known for itsextreme dryness up to 2003 therewas little interest in explor-ing and characterizing its potentialmicrobial ecosystems as itwas generally supposed to be sterile Ten years later microbiallife has been found in most if not all of its habitats fromhigh thermal springs on the Andes Mountains to caves of theCoastal Range thus building a yet ongoing descriptive stage


of extant microbial ecosystemsTherefore it is not surprisingthat the technological stage of research is just beginning

As previously mentioned the Atacama Desert is uniqueas it has been the most arid place on Earth for a very longtime imposing the same selection pressure over the life formsthat arrived and then coevolved with it Fittingly all reportsto date have shown that these species are unique in the waythe capture store and use water tolerate solar radiation highsaline conditions and low soil nutrients [7 74]Thus with theexception of copper bioleaching now a multimillion dollarindustry we believe there is an immense biotechnologicalpotential waiting to be discovered and developed in relationto the tolerance to the aforementioned abiotic stresses

Most groups now are still reporting various degrees oftolerance to abiotic stresses in the frame of basic research(extreme environments and astrobiology in particular) andwe foresee that during the next years the detailed understand-ing of the physiological and molecular mechanisms involvedin the many abiotic stress tolerances shown by these speciesshould increase to a great extent (see [13] eg) ldquoOmicsrdquotechniques like genomics proteomics and metabolomicsand high-throughput technologies will be key in elucidatingprocesses and mechanisms involved in these tolerances andthen in identifying and characterizing key molecules ofpotential use

In the case of bioleaching we envision that new bacte-rial and archaeal strains will appear in the market Tailor-made combinations of mine-specific strains will probably beisolated characterized and patented in order to maximizethe dissolution of copper from the particular complexityof minerals characteristic of each place In addition otherproperties of the mine may be taken into account in thedetermination of the characteristics of the strainmixture likewater quality soil temperature and so forth

In the case of biomolecules of interest for the biomedicalindustry there are already a handful of groups charac-terizing potentially interesting biomolecules from bacterialstrains isolated from the hyperarid areas and hypersalinelagoons of the Atacama Desert biomolecules which havejust been identified and their activities preliminary testedThese isolates are few and are representatives of a very smallfraction of the habitats of the Atacama so novel strainsand metabolites will certainly appear in the near futureMicroorganisms of the dry core of the Atacama will be ofparticular interest as we expect that these species beingsubjected to the most extreme conditions should producea number of biomolecules involved in the competition forscarce resources

With the increasing pressure of finding new drugs ableto handle antibiotic-resistant pathogens [75] extreme envi-ronments are now being investigated in detail [76] and theAtacama Desert given its unique peculiarities may be aprime place to explore

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

References

[1] C P McKay E I Friedmann B Gomez-Silva L Caceres-Villanueva D T Andersen and R Landheim ldquoTemperatureand moisture conditions for life in the extreme arid region ofthe atacama desert four years of observations including the ElNino of 1997-1998rdquoAstrobiology vol 3 no 2 pp 393ndash406 2003

[2] J F Reynolds P R Kemp K Ogle and R J FernandezldquoModifying the rsquopulse-reserversquo paradigm for deserts of NorthAmerica precipitation pulses soil water and plant responsesrdquoOecologia vol 141 no 2 pp 194ndash210 2004

[3] C J TuckerH EDregne andWWNewcomb ldquoExpansion andcontraction of the Sahara desert from 1980 to 1990rdquo Science vol253 no 5017 pp 299ndash300 1991

[4] UnitedNations Environment Programme (UNEP)WorldAtlasof Desertification 1992

[5] A J Hartley G Chong J Houston and A E Mather ldquo150million years of climatic stability evidence from the AtacamaDesert northern Chilerdquo Journal of the Geological Society vol162 no 3 pp 421ndash424 2005

[6] J Houston and A J Hartley ldquoThe central andean west-sloperainshadow and its potential contribution to the origin ofhyper-aridity in the Atacama Desertrdquo International Journal ofClimatology vol 23 no 12 pp 1453ndash1464 2003

[7] A Azua-Bustos C Urrejola and R Vicuna ldquoLife at the dryedgemicroorganisms of theAtacamaDesertrdquoTheFEBS Lettersvol 586 no 18 pp 2939ndash2945 2012

[8] A Azua-Bustos C Gonzalez-Silva R A Mancilla et alldquoHypolithic cyanobacteria supported mainly by fog in thecoastal range of the Atacama DesertrdquoMicrobial Ecology vol 61no 3 pp 568ndash581 2011

[9] E K Costello S R P Halloy S C Reed P Sowell and S KSchmidt ldquoFumarole-supported islands of biodiversity within ahyperarid high-elevation landscape on socompa volcano punade atacama andesrdquo Applied and Environmental Microbiologyvol 75 no 3 pp 735ndash747 2009

[10] JWierzchos CAscaso andC PMcKay ldquoEndolithic cyanobac-teria in halite rocks from the hyperarid core of the AtacamaDesertrdquo Astrobiology vol 6 no 3 pp 415ndash422 2006

[11] A Azua-Bustos C Gonzalez-Silva L Salas R E Palma and RVicuna ldquoA novel subaerial Dunaliella species growing on cavespiderwebs in the Atacama Desertrdquo Extremophiles vol 14 no5 pp 443ndash452 2010

[12] A Azua-Bustos C Gonzalez-Silva R A Mancilla et alldquoAncient photosynthetic eukaryote biofilms in an AtacamaDesert coastal caverdquo Microbial Ecology vol 58 no 3 pp 485ndash496 2009

[13] A Azua-Bustos J Zuniga C Arenas-Fajardo M OrellanaL Salas and R Vicuna ldquoGloeocapsopsis AAB1 an extremelydesiccation-tolerant cyanobacterium isolated from the Ata-cama Desertrdquo Extremophiles vol 18 no 1 pp 61ndash74 2014

[14] P L Bergquist H W Morgan and D Saul ldquoSelected enzymesfromextreme thermophileswith applications in biotechnologyrdquoCurrent Biotechnology vol 3 no 1 pp 45ndash59 2014

[15] D P Kelly and A P Wood ldquoReclassification of some speciesofThiobacillus to the newly designated genera Acidithiobacillusgen nov Halothiobacillus gen nov and Thermithiobacillusgen novrdquo International Journal of Systematic and EvolutionaryMicrobiology vol 50 no 2 pp 511ndash516 2000

[16] P Norris ldquoAcidophile diversity in mineral sulfide oxidationrdquoin Biomining D Rawlings and B Johnson Eds pp 199ndash216Springer Berlin Germany 2007


[17] A Schippers ldquoMicroorganisms involved in bioleaching andnucleic acid-based molecular methods for their identificationand quantificationrdquo inMicrobial Processing of Metal Sulfides EDonati and W Sand Eds pp 3ndash33 Springer Dordrecht TheNetherlands 2007

[18] E M Domic-Mihovilovic ldquoA review of the development andcurrent status of copper bioleaching operations in Chile 25years of successful commercial implementationrdquo in BiominingD E Rawlings and B D Johnson Eds pp 81ndash95 SpringerBerlin Germany 2007

[19] J C Gentina and F Acevedo ldquoApplication of bioleaching tocoppermining inChilerdquoElectronic Journal of Biotechnology vol16 no 3 pp 1ndash16 2013

[20] K P Drees J W Neilson J L Betancourt et al ldquoBacterialcommunity structure in the hyperarid core of the AtacamaDesert ChilerdquoApplied and EnvironmentalMicrobiology vol 72no 12 pp 7902ndash7908 2006

[21] H Korehi M Blothe M A Sitnikova B Dold and ASchippers ldquoMetal mobilization by iron- and sulfur-oxidizingbacteria in a multiple extreme mine tailings in the AtacamaDesert Chilerdquo Environmental Science amp Technology vol 47 no5 pp 2189ndash2196 2013

[22] C M Zammit S Mangold V Rao Jonna et al ldquoBioleaching inbrackish waters-effect of chloride ions on the acidophile pop-ulation and proteomes of model speciesrdquo Applied Microbiologyand Biotechnology vol 93 no 1 pp 319ndash329 2012

[23] T Sugio A Miura P A Parada Valdecantos and R BadillaOhlbaum ldquoBacteria strain Wenelen DSM 16786 use of saidbacteria for leaching of ores or concentrates containingmetallicsulfide mineral species and leaching processes based on the useof said bacteria or other publications mixtures that contain saidbacteriardquo United States Patent US 7601530 B2 2009

[24] A Ohata M Manaba and P A Parada Valdecantos ldquoSulfur-oxidizing bacteria and their use in bioleaching processes forsulfured coppermineralsrdquoUnited States Patent noUS 7700343B2 2009

[25] A Ohata M Manabe and P A Parada ldquoSulfur-oxidizingbacteria and their use in bioleaching processes for sulfuredcopper mineralsrdquo United States Patent No US 7700343 2010

[26] T Sugio A Miura P A Parada and R Badilla ldquoBacteriastrain Wenelen DSM 16786 use of said bacteria for leaching ofores or concentrates containing metallic sulfide mineral speciesand leaching processes based on the use of said bacteria ormixtures that contain said bacteriardquo United States Patent NoUS 7601530 2009

[27] G Levican J A Ugalde N Ehrenfeld A Maass and P ParadaldquoComparative genomic analysis of carbon and nitrogen assim-ilation mechanisms in three indigenous bioleaching bacteriapredictions and validationsrdquo BMC Genomics vol 9 article 5812008

[28] P Martınez S Galvez N Ohtsuka et al ldquoMetabolomic study ofChilean biomining bacteriaAcidithiobacillus ferrooxidans strainWenelen and Acidithiobacillus thiooxidans strain LicanantayrdquoMetabolomics vol 9 no 1 pp 247ndash257 2013

[29] R E Cameron D R Gensel and G B Blank ldquoSoil studiesmdashdesert microflora XII abundance of microflora in soil samplesfrom the Chile Atacama Desertrdquo in Space Programs Summaryvol 4 pp 37ndash38 Jet Propulsion Laboratory 1966

[30] R Navarro-Gonzalez F A Rainey P Molina et al ldquoMars-likesoils in theAtacamaDesert Chile and the dry limit ofmicrobialliferdquo Science vol 302 no 5647 pp 1018ndash1021 2003

[31] H Onaka ldquoBiosynthesis of heterocyclic antibiotics in actino-mycetes and an approach to synthesize the natural compoundsrdquoActinomycetologica vol 20 no 2 pp 62ndash71 2006

[32] C K Okoro R Brown A L Jones et al ldquoDiversity of culturableactinomycetes in hyper-arid soils of the AtacamaDesert ChilerdquoAntonie van Leeuwenhoek International Journal of General andMolecular Microbiology vol 95 no 2 pp 121ndash133 2009

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[34] M E Rateb W E Houssen W T A Harrison et al ldquoDiversemetabolic profiles of a Streptomyces strain isolated fromahyper-arid environmentrdquo Journal of Natural Products vol 74 no 9 pp1965ndash1971 2011

[35] M E RatebW EHoussenMArnold et al ldquoChaxamycins AmdashD bioactive ansamycins from a hyper-arid desert Streptomycessprdquo Journal of Natural Products vol 74 no 6 pp 1491ndash14992011

[36] J Nachtigall A Kulik S Helaly et al ldquoAtacamycins A-C 22-membered antitumor macrolactones produced by Streptomycessp C38rdquo Journal of Antibiotics vol 64 no 12 pp 775ndash780 2011

[37] Y H Jeon Y Heo C M Kim et al ldquoPhosphodiesteraseoverview of protein structures potential therapeutic applica-tions and recent progress in drug developmentrdquo Cellular andMolecular Life Sciences vol 62 no 11 pp 1198ndash1220 2005

[38] M Leiros E Alonso J A Sanchez et al ldquoMitigation ofROS insults by Streptomyces secondary metabolites in primarycortical neuronsrdquo ACS Chemical Neuroscience vol 15 no 1 pp71ndash80 2014

[39] D Schulz P Beese B Ohlendorf et al ldquoAbenquines A-DAminoquinone derivatives produced by Streptomyces sp strainDB634rdquo Journal of Antibiotics vol 64 no 12 pp 763ndash768 2011

[40] C Vezina A Kudelski and S N Sehgal ldquoRapamycin (AY22989) a new antifungal antibiotic I Taxonomy of the produc-ing streptomycete and isolation of the active principlerdquo Journalof Antibiotics vol 28 no 10 pp 721ndash726 1975

[41] B K Law ldquoRapamycin an anti-cancer immunosuppressantrdquoCritical Reviews in OncologyHematology vol 56 no 1 pp 47ndash60 2005

[42] F Neff D Flores-Dominguez D P Ryan et al ldquoRapamycinextends murine lifespan but has limited effects on agingrdquoJournal of Clinical Investigation vol 123 no 8 pp 3272ndash32912013

[43] M V Blagosklonny ldquoRapamycin extends life- and health spanbecause it slows agingrdquo Aging vol 5 no 8 pp 592ndash598 2013

[44] V L Campos G Escalante J Yanez C A Zaror and MA Mondaca ldquoIsolation of arsenite-oxidizing bacteria from anatural biofilm associated to volcanic rocks of Atacama DesertChilerdquo Journal of Basic Microbiology vol 49 no 1 pp S93ndashS972009

[45] M Kim J Nriagu and S Haack ldquoCarbonate ions and arsenicdissolution by groundwaterrdquo Environmental Science and Tech-nology vol 34 no 15 pp 3094ndash3100 2000

[46] K Hrynkiewicz and C Baum ldquoApplication of microorganismsin bioremediation of environment from heavy metalsrdquo inEnvironmental Deterioration and Human Health A MalikE Grohmann and R Akhtar Eds pp 215ndash227 SpringerAmsterdam The Netherlands 2014

[47] S Yamamura and S Amachi ldquoMicrobiology of inorganicarsenic from metabolism to bioremediationrdquo Journal of Bio-science and Bioengineering vol 118 no 1 pp 1ndash9 2014


[48] J H Huang ldquoImpact of microorganisms on arsenic biogeo-chemistry a reviewrdquo Water Air amp Soil Pollution vol 225 no2 article 1848 2014

[49] P L Smedley and D G Kinniburgh ldquoA review of the sourcebehaviour and distribution of arsenic in natural watersrdquoAppliedGeochemistry vol 17 no 5 pp 517ndash568 2002

[50] D K Nordstrom ldquoWorldwide occurrences of arsenic in groundwaterrdquo Science vol 296 no 5576 pp 2143ndash2145 2002

[51] D D Caceres P Pino N Montesinos E Atalah H Amigoand D Loomis ldquoExposure to inorganic arsenic in drinkingwater and total urinary arsenic concentration in a Chileanpopulationrdquo Environmental Research vol 98 no 2 pp 151ndash1592005

[52] S Shen X F Li W R Cullen M Weinfeld and X C LeldquoArsenic binding to proteinsrdquo Chemical Reviews vol 113 no 10pp 7769ndash7790 2013

[53] G Escalante V L Campos C Valenzuela J Yanez C Zarorand M A Mondaca ldquoArsenic resistant bacteria isolated fromarsenic contaminated river in the Atacama Desert (Chile)rdquoBulletin of Environmental Contamination and Toxicology vol83 no 5 pp 657ndash661 2009

[54] V L Campos C Valenzuela P Yarza et al ldquoPseudomonasarsenicoxydans sp nov an arsenite-oxidizing strain isolatedfrom the Atacama desertrdquo Systematic and AppliedMicrobiologyvol 33 no 4 pp 193ndash197 2010

[55] A S Butt and A Rehman ldquoIsolation of arsenite-oxidizingbacteria from industrial effluents and their potential use inwastewater treatmentrdquo World Journal of Microbiology andBiotechnology vol 27 no 10 pp 2435ndash2441 2011

[56] A Das S H Yoon S H Lee J Y Kim D K Oh and SW KimldquoAn update on microbial carotenoid production application ofrecent metabolic engineering toolsrdquo Applied Microbiology andBiotechnology vol 77 no 3 pp 505ndash512 2007

[57] J A del Campo M Garcıa-Gonzalez and M G GuerreroldquoOutdoor cultivation of microalgae for carotenoid produc-tion current state and perspectivesrdquo Applied Microbiology andBiotechnology vol 74 no 6 pp 1163ndash1174 2007

[58] B Demmig-Adams and W W Adams III ldquoAntioxidants inphotosynthesis and human nutritionrdquo Science vol 298 no5601 pp 2149ndash2153 2002

[59] G Britton S Liaaen-Jensen and H Pfander CarotenoidsHandbook Birkhaauser Basel Switzerland 2004

[60] A Das S Yoon S Lee J Kim D Oh and S Kim ldquoAnupdate on microbial carotenoid production application ofrecent metabolic engineering toolsrdquo Applied Microbiology andBiotechnology vol 77 no 3 pp 505ndash512 2007

[61] MM Ciccone F CorteseM Gesualdo et al ldquoDietary intake ofcarotenoids and their antioxidant and anti-inflammatory effectsin cardiovascular caremediators of inflammationrdquoMediators ofInflammation vol 2013 Article ID 782137 11 pages 2013

[62] J Fiedor J and K Burda ldquoPotential role of carotenoids asantioxidants in human health and diseaserdquoNutrients vol 6 no2 pp 466ndash488 2014

[63] L H Reyes J M Gomez and K C Kao ldquoImprovingcarotenoids production in yeast via adaptive laboratory evolu-tionrdquoMetabolic Engineering vol 21 no 1 pp 26ndash33 2014

[64] A Oren ldquoA hundred years of Dunaliella research 1905ndash2005rdquoSaline Systems vol 1 no 2 2005

[65] W Fu G Paglia M Magnusdottir et al ldquoEffects of abioticstressors on lutein production in the greenmicroalgaDunaliellasalinardquoMicrobial Cell Factories vol 13 no 3 pp 1ndash9 2014

[66] A Ben-Amotz ldquoDunaliella 120573-carotene from science to com-mercerdquo in Enigmatic Microorganisms and Life in ExtremeEnvironments J Seckbach Ed pp 399ndash410 Kluwer AcademicPublishers Dordrecht The Netherlands 1999

[67] A Ben-Amotz and M Avron ldquoThe role of glycerol in theosmotic regulation of the halophilic alga Dunaliella parvardquoPlant Physiology vol 51 no 5 pp 875ndash878 1973

[68] P Araneda C Jimenez and B Gomez-Silva ldquoMicroalgae fromNorthern Chile III Growth and beta carotene content of threeisolates of Dunaliella salina from the Atacama Desertrdquo Revistade Biologıa Marina y Oceanografıa vol 27 no 2 pp 157ndash1621992

[69] P I Gomez and M A Gonzalez ldquoGenetic variation amongseven strains of Dunaliella salina (Chlorophyta) with industrialpotential based on RAPD banding patterns and on nuclear ITSrDNA sequencesrdquo Aquaculture vol 233 no 1ndash4 pp 149ndash1622004

[70] A S Cifuentes M Gonzalez O Parra M Zu and M ZunigaldquoCulture of strains of Dunaliella salina (Teodoresco 1905) indifferent media under laboratory conditionsrdquo Revista Chilenade Historia Natural vol 69 no 1 pp 105ndash112 1996

[71] D Arias-Forero G Hayashida M Aranda et al ldquoProtocolfor maximizing the triglycerides-enriched lipids productionfrom Dunaliella salina SA32007 biomass isolated from theSalar de Atacama (Northern Chile)rdquoAdvances in Bioscience andBiotechnology vol 4 no 8 pp 830ndash839 2013

[72] W Fu O Guethmundsson G Paglia et al ldquoEnhancement ofcarotenoid biosynthesis in the greenmicroalgaDunaliella salinawith light-emitting diodes and adaptive laboratory evolutionrdquoAppliedMicrobiology and Biotechnology vol 97 no 6 pp 2395ndash2403 2013

[73] D Geng Y Han Y Wang et al ldquoConstruction of a system forthe stable expression of foreign genes in Dunaliella salinardquoActaBotanica Sinica vol 46 no 3 pp 342ndash346 2004

[74] A Azua-Bustos C Gonzalez-Silva C Arenas-Fajardo and RVicuna ldquoExtreme environments as potential drivers of conver-gent evolution by exaptation theAtacamaDesertCoastal Rangecaserdquo Frontiers in Microbiology vol 3 article 426 2012

[75] B Cannon ldquoMicrobiology resistance fightersrdquoNature vol 509no 7498 pp S6ndashS8 2014

[76] A Tasiemski S Jung C Boidin-Wichlacz et al ldquoCharacteri-zation and function of the first antibiotic isolated from a ventorganism the extremophile metazoan Alvinella pompejanardquoPLoS ONE vol 9 no 4 Article ID e95737 2014

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

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International Journal of

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Zoology


Molecular Biology International

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GenomicsInternational Journal of

Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014


BioinformaticsAdvances in

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Evolutionary BiologyInternational Journal of



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Advances in

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Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational



Enzyme Research



Microbiology


(a) (b)

(c)

Figure 1 Examples of habitats of the Atacama Desert from where biotechnological applications have been derived or used (a) The centralvalley the hyperarid core of the Atacama Desert (b) Heap bioleaching at Radomiro Tomic an open pit copper mine owned by the ChileanCopper Corporation (Codelco) Note the copper rich blue-green solution obtained from the heaps (c) The Loa River a typical arsenic richriver of the Atacama Desert Image credits Panels A and C Armando Azua-Bustos Panel B Armando Azua Aroz

2 Applications Derived from Members ofthe Bacteria Domain

Copper Bioleaching Copper bioleaching or ldquobiominingrdquoallowed the usage of insoluble copper sulphides and oxidesthrough hydrometallurgy as opposed to the traditionaltechnology of pyrometallurgy Compared to pyrometallurgybioleaching has the advantage of being a simpler processrequiring less energy and equipments (Figure 1(b)) In addi-tion bioleaching does not produce sulfur dioxide emissionsan important factor for the Chilean mining towns whichwere usually built alongside the extracting operations inChile (most of which are located in the Atacama Desert)Bioleaching also offered a better treatment of low grade(again the usual case in Atacama copper ores) or wasteores and in many cases it is the only way to treat themLow-grade ores (06 and less) are abundant in Chilebut their processing by pyrometallurgy in most cases isnot economical Through bioleaching copper was able tobe extracted from ore minerals like chalcopyrite (CuFeS2)with the crucial contribution of chemolithotrophic microbialspecies extremely tolerant to low pH which use the reducedsulphur as an energy source The most known of thesemicroorganisms is Acidithiobacillus ferrooxidans [15] butother species like Leptospirillum ferrooxidans Sulfobacillusacidophilus and Acidimicrobium ferrooxidans are thought toalso participate in the bioleaching process [16 17]

In Chile the first mine that introduced bioleaching wasSociedad Minera Pudahuel (a copper mine not located inthe Atacama) in the 1980s Today this process is extensivelyused in the Chilean copper mining industry [18 19] reachingover 16 million tons of copper per year [19] It has beenestimated that Chilersquos copper actual reserves would increaseup to 50 if all copper sulphides could be economicallytreated by bioleaching [19]

Acidithiobacillus ferrooxidans has been identified in dif-ferent places of the Atacama Desert [20 21] Some of thesespecies have been found in sulfidic mine tailings dumps inthe marine shore at Chanaral Bay [21] located at the CoastalRange of the Atacama This is of particular interest as thesespecies were found to be halotolerant iron oxidizers activeat NaCl concentrations up to 1M in enrichment culturesHigh concentrations of chloride ions inhibit the growth of theacidophilic microorganisms traditionally used in biomining[22] Thus the finding of halotolerant bioleaching specieswould allow the use of seawater for biomining operations inthe future a very important advancement in a region wherewater availability has always been extremely low

Bioleaching strains found in the Atacama Desert havebeen recently patented as is the case of Acidithiobacillus fer-rooxidans strainWenelenDSM 16786 [23] andAcidithiobacil-lus thiooxidans strain Licanantay DSM 17318 [24] (US Patentnumbers 7601530 and 7700343) Both strains showedimproved oxidizing activity when compared to standard























4 Final Comments











References






















































































Volume 2014

Zoology





Volume 2014


















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology























4 Final Comments











References






















































































Volume 2014

Zoology





Volume 2014


















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology










References






















































































Volume 2014

Zoology





Volume 2014


















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology






































































Volume 2014

Zoology





Volume 2014


















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology

Biotechnological applications derived from microorganisms of the Atacama Desert

Documents

Transcript of Biotechnological applications derived from microorganisms of the Atacama Desert