Parageobacillus Thermantarcticus, an Antarctic Cell Factory: from Crop Residue Valorization by Green Chemistry to Astrobiology Studies
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diversity Review Parageobacillus thermantarcticus, an Antarctic Cell Factory: From Crop Residue Valorization by Green Chemistry to Astrobiology Studies Ilaria Finore 1 , Licia Lama 1, Paola Di Donato 1,2, Ida Romano 1, Annabella Tramice 1, Luigi Leone 1, Barbara Nicolaus 1 and Annarita Poli 1,* 1 Institute of Biomolecular Chemistry, Consiglio Nazionale delle Ricerche, Via Campi Flegrei 34, 80078 Pozzuoli, Italy 2 Department of Science and Technology, University of Naples Parthenope, Centro Direzionale, Isola C4, 80143 Naples, Italy * Correspondence: [email protected] Received: 13 May 2019; Accepted: 4 August 2019; Published: 7 August 2019 Abstract: Knowledge of Antarctic habitat biodiversity, both marine and terrestrial, has increased considerably in recent years, causing considerable development in the studies of life science related to Antarctica. In the Austral summer 1986–1987, a new thermophilic bacterium, Parageobacillus thermantarcticus strain M1 was isolated from geothermal soil of the crater of Mount Melbourne (74◦220 S, 164◦400 E) during the Italian Antarctic Expedition. In addition to the biotechnological potential due to the production of exopolysaccharides and thermostable enzymes, successful studies have demonstrated its use in the green chemistry for the transformation and valorization of residual biomass and its employment as a suitable microbial model for astrobiology studies. The recent acquisition of its genome sequence opens up new opportunities for the use of this versatile bacterium in still unexplored biotechnology sectors. Keywords: Parageobacillus thermantarcticus; mount melbourne Antarctica; xylanase; beta-xylosidase; xylose/glucose isomerase; protease; exopolysaccharide; draft genoma; astrobiology; xylooligosaccharides 1. Introduction The knowledge of thermophiles biodiversity could be very useful for the discovery of new molecules and/or more thermostable biocatalysts with thermophilic and thermostability properties superior to those currently known and in use [1,2]. Recent exploitations have clearly shown that thermophilic microorganisms are industrial providers of novel catalysts, and in some cases, these enzymes have been cloned and expressed in suitable mesophilic hosts [1,3]. The biggest part of thermophiles studied belongs to the genus Geobacillus, and several strains have been found in thermophilic and mesophilic environments [1,4]. The development of extremophiles from geothermal areas, as a resource for novel thermostable enzymes, has received attention even in Antarctica, where the presence of thermophiles has been indicated by the discovery of several geothermal areas [5]. Thermophilic enzymes (also called thermozymes) work and remain stable at high temperatures, and they are to be preferred to the mesophilic counterpart for their biotechnological potential [6]. In view of this, a thermophilic bacterium, Parageobacillus thermantarcticus, (DSM 9572T) strain M1 [7,8], isolated from geothermal soil of Mount Melbourne (74◦220 S, 164◦400 E) in Antarctica (Italian Antarctica Expedition during the Austral summer 1986–1987), was characterized for the production of thermostable enzymatic activities such as an extracellular xylanase, a beta-xylosidase, an intracellular xylose/glucose isomerase, and a protease. Diversity 2019, 11, 128; doi:10.3390/d11080128 www.mdpi.com/journal/diversity Diversity 2019, 11, x FOR PEER REVIEW 2 of 23 Diversity 2019, 11, 128 2 of 23 The interesting enzymatic pathways present in P. thermantarcticus make this Antarctic thermophileThe interesting of great enzymatic potential pathwaysin biotechnological present in P.applications, thermantarcticus not makeonly for this industrial Antarctic thermophilebiocatalysis butof great also for potential bioprocessing in biotechnological aims. In fact, applications, the optimization not onlyof enzymatic for industrial procedures biocatalysis for the butconversion also for ofbioprocessing waste lignocellulosic aims. In materials fact, the optimization in high added of value enzymatic molecules procedures using the for xylanolytic the conversion enzymatic of waste set oflignocellulosic P. thermantarcticus materials produced in high extremely added valueinteresting molecules results using and was the recently xylanolytic reported enzymatic [9,10]. These set of P.enzymes, thermantarcticus which wereproduced involved extremely in the enzymatic interesting digestions results of and hemicellulolitic was recently reportedfraction obtained [9,10]. These from rhizomesenzymes, whichof Arundo were donax involved and inthe the waste enzymatic stems digestionsand leaves of biomasses hemicellulolitic of Cynara fraction cardunculus obtained, have from beenrhizomes used of forArundo the bioconversion donax and the of waste agroresidues stems and into leaves xylo-oligomers biomasses ofandCynara fermentable cardunculus sugars., have been usedMoreover, for the bioconversion it was demonstrated of agroresidues that into P. xylo-oligomersthermantarcticus and produces fermentable two sugars.exopolysaccharides (calledMoreover, EPS 1 and it wasEPS demonstrated2) that are responsible that P. thermantarcticus for typical mucousproduces colonies. two These exopolysaccharides EPSs were produced (called usingEPS 1 andmannose EPS 2) as that a sole are responsiblecarbon and forenergy typical source mucous with colonies. a yield Theseof 400 EPSs mg/L. were Nuclear produced magnetic using resonancemannoseas spectra a sole carbonestablished and energythat EPS source 1 was with a axantan yield of polymer, 400 mg/L. while Nuclear EPS magnetic 2 was a resonance mannan polysaccharidespectra established [11]. that EPS 1 was a xantan polymer, while EPS 2 was a mannan polysaccharide [11]. P. thermantarcticus hashas also also been been used used as asa biologic a biologicalal model model for forastrobiology, astrobiology, i.e., i.e.,the multidisciplinarythe multidisciplinary approach approach to the to study the studyof origin of and origin evolution and evolution of life on of Earth life onand Earth in the and Universe. in the ItUniverse. has been It demonstrated has been demonstrated that either that the either viable the cells viable or the cells spores or the of spores P. thermantarcticus of P. thermantarcticus to spaceto simulationspace simulation are interesting are interesting for the for issue the issue of the of theorigin origin of oflife life [12–14]. [12–14 ].Indeed, Indeed, the the finding finding of of bacterial bacterial species fit fit to survive in space parameters open open new new scenarios scenarios for for the the so-called so-called panspermia panspermia theory. theory. According to this theory, life on Earth could have originated from bacterial species from other places transported by solar pr pressure.essure. The The identification identification of of bacteria bacteria like like P. thermantarcticus that potentially could survive to the space transport is oneone main key point to support this theory.theory. Recently, thanksthanks to to participation participation to “Theto “The Genomic Genomic Encyclopedia Encyclopedia of Bacteria of Bacteria and Archaea and Archaea (GEBA) (GEBA)III Project”, III Project”, a project a of project the Community of the Community Science Program Science Program (CSP) of the(CSP) DOE of the Joint DOE Genomes Joint Genomes Institute, Institute,the draft genomicthe draft sequencegenomic sequence of P. thermantarcticus of P. thermantarcticususing the using Illumina the technologyIllumina technology has been obtained.has been Withobtained. the availableWith the genome available sequence, genome the sequence biotechnology, the biotechnology potential and potential the use of andP. thermantarcticus the use of P. willthermantarcticus increase. For will example, increase. like For a factory, example,P. thermantarcticus like a factory,could P. thermantarcticus convert unexplored could feedstocks convert unexploredinto useful productsfeedstocks such into as useful biobased products chemicals, such fromas biobased renewable chemicals, resources, from for renewable biofuels production, resources, forbioplastic biofuels materials production, development, bioplastic etc. materials The increase develo of geneticpment, tools etc. isThe a requirement increase of for genetic high-throughput tools is a requirementengineering. for There high-throughput is the opportunity engineering. to explore Ther ande is exploit the opportunity the physiology to explore of a really and exploit interesting the physiologybacterium likeof aP. really thermantarcticus interesting :bacterium This will like necessarily P. thermantarcticus involve an: This integrated will necessarily approach involve of various an integrateddisciplines approach (Figure1)[ of15 various]. disciplines (Figure 1) [15]. Figure 1. Parageobacillus thermantarcticus: a microbial cell factory. Figure 1. Parageobacillus thermantarcticus: a microbial cell factory. Diversity 2019, 11, 128 3 of 23 2. Phylogenomic Re-Assessment of Bacillus thermoantarcticus to Parageobacillus thermantarcticus It was 1996 when Nicolaus et al. [8] described the isolation and the taxonomic description of a new Antarctic thermophilic species of Bacillus strain M1, isolated from the geothermal soil of Mount Melbourne, for which the name Bacillus thermoantarcticus was indicated. The name thermoantarcticus was subsequently corrected in thermantarcticus (therm.ant.arc’ti.cus. Gr. n. thermệ heat; L. masc. adj. antarcticus southern, belonging to Antarctica; N.L. masc. adj. thermantarcticus, a thermophile from Antarctica)