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Diversity of Cultivated Aerobic Poly-Hydrolytic Bacteria in Saline Alkaline Soils

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Diversity of Cultivated Aerobic Poly-Hydrolytic Bacteria in Saline Alkaline Soils A peer-reviewed version of this preprint was published in PeerJ on 25 September 2017. View the peer-reviewed version (peerj.com/articles/3796), which is the preferred citable publication unless you specifically need to cite this preprint. Sorokin DY, Kolganova TV, Khijniak TV, Jones BE, Kublanov IV. 2017. Diversity of cultivated aerobic poly-hydrolytic bacteria in saline alkaline soils. PeerJ 5:e3796 https://doi.org/10.7717/peerj.3796 Diversity of cultivated aerobic poly-hydrolytic bacteria in saline alkaline soils Dmitry Y. Sorokin 1, 2 , Tatiana V. Kolganova 3 , Tatiana V. Khijniak 1 , Brian E. Jones 4 , Ilya V. Kublanov Corresp. 1, 5 1 Winogradsky Institute of Microbiology, Research Centre of Biotechnology, Russian Academy of Sciences, Moscow, Russia 2 Department of Biotechnology, Delft University of Technology, Delft, Netherlands 3 Institute of Bioengineering, Research Centre of Biotechnology, Russian Academy of Sciences, Moscow, Russia 4 DuPont Industrial Biosciences/Genencor International BV, Leiden, Netherlands 5 Immanuel Kant Baltic Federal University, Kaliningrad, Russia Corresponding Author: Ilya V. Kublanov Email address: [email protected] Alkaline saline soils known also as “soda solonchaks” represent a natural soda habitat which differed from soda lake sediments by higher aeration and lower humidity. The microbiology of soda soils, in contrast to the more intensively studied soda lakes, remains poorly explored. In this work we present information on the diversity of culturable aerobic haloalkalitolerant bacteria with various hydrolytic activities from soda soils at different locations in Central Asia and Africa. In total, 180 isolates were obtained by using media with various polymers at pH 10 and 0.6 M total Na+. According to the 16S rRNA gene sequences analysis, most of the isolates belonged to Firmicutes and Actinobacteria. Most isolates possessed multiple hydrolytic activities, including endoglucanase, xylanase, amylase and protease. The pH profiling of selected representatives of actinobacteria and endospore-forming bacteria showed, that the former were facultative alkaliphiles, while the latter were mostly obligate alkaliphiles. The hydrolases of both groups were active at a broad pH range from 6 to 11. Overall, this work demonstrated the presence of a rich hydrolytic bacterial community in soda soils which might be explored further for production of haloalkalistable hydrolases. PeerJ Preprints | https://doi.org/10.7287/peerj.preprints.3038v1 | CC BY 4.0 Open Access | rec: 21 Jun 2017, publ: 21 Jun 2017 1 Diversity of cultivated aerobic poly-hydrolytic bacteria in saline alkaline soils 2 3 4 Dmitry Y. Sorokin1,2, Tatiana V. Kolganova3, Tatiana V. Khijniak1, B. E. Jones4, I. V. 5 Kublanov1,5 6 7 1Winogradsky Institute of Microbiology, Research Centre of Biotechnology, Russian Academy 8 of Sciences, Leninskii Prospect 33/2, 119071 Moscow, Russia 9 10 2Department of Biotechnology, Delft University of Technology, Delft, The Netherlands 11 12 3Institute of Bioengineering, Research Centre of Biotechnology, Russian Academy of Sciences, 13 Moscow, Russia 14 15 4DuPont Industrial Biosciences/Genencor International BV, Leiden, The Netherlands 16 17 5Immanuel Kant Baltic Federal University, Kaliningrad, Russia. 18 19 20 21 22 23 24 25 26 27 28 29 30 Nucleotide sequence accession number: GenBank/EMBL accession numbers of the 16S rRNA 31 determined in this study are KY775645-KY775672. 32 34 Abstract 35 Alkaline saline soils known also as “soda solonchaks” represent a natural soda habitat which 36 differed from soda lake sediments by higher aeration and lower humidity. The microbiology of 37 soda soils, in contrast to the more intensively studied soda lakes, remains poorly explored. In this 38 work we present information on the diversity of culturable aerobic haloalkalitolerant bacteria 39 with various hydrolytic activities from soda soils at different locations in Central Asia and 40 Africa. In total, 180 isolates were obtained by using media with various polymers at pH 10 and 41 0.6 M total Na+. According to the 16S rRNA gene sequences analysis, most of the isolates 42 belonged to Firmicutes and Actinobacteria. Most isolates possessed multiple hydrolytic 43 activities, including endoglucanase, xylanase, amylase and protease. The pH profiling of selected 44 representatives of actinobacteria and endospore-forming bacteria showed, that the former were 45 facultative alkaliphiles, while the latter were mostly obligate alkaliphiles. The hydrolases of both 46 groups were active at a broad pH range from 6 to 11. Overall, this work demonstrated the 47 presence of a rich hydrolytic bacterial community in soda soils which might be explored further 48 for production of haloalkalistable hydrolases. 49 50 Keywords: soda solonchak soils, aerobic hydrolytics, haloalkaliphilic, Actinobacteria, Bacillus 51 52 Running title: 53 54 poly-hydrolytic bacteria from solonchaks 56 Introduction 57 58 For a long time already alkaliphilic aerobic hydrolytic bacteria have attracted attention as sources 59 of alkali-stable hydrolases for various industrial applications, primarily enzymatic laundry 60 detergents (reviewed by: Horikoshi 2004; 2006; Fujinami & Fujisawa, 2010; Grant & Heaphy, 61 2010; Sarethy et al., 2011; Zhao et al., 2014; Mamo & Mattiasson, 2016). Most of this research 62 was done with non-halotolerant Bacillus species producing alkalistable proteases, amylases and 63 endoglucanases. In contrast, only a few salt tolerant alkaliphilic hydrolytics have been isolated 64 and characterized from saline alkaline (soda) lakes. So far, the majority of known soda lake 65 hydrolytics are found among anaerobic fermenters. A low salt-tolerant Clostridium 66 alkalicellulosi is so far the only truly anaerobic cellulolytic bacterium able to grow on crystalline 67 cellulose found in soda lakes (Zhilina et al., 2005). Pectin utilization for growth at haloalkaline 68 conditions has been demonstrated in two fermentative anaerobic haloalkaliphiles: Natronoflexus 69 pectinovorans (Bacteriodetes) and Natranaerovirga hydrolytica (Clostridia) at moderate and 70 high salinity, respectively (Sorokin et al., 2011; 2012a). Two groups of fermentative 71 haloalkaliphilic bacteria narrowly specialized in the utilization of chitin as a growth substrate 72 have been found in hypersaline soda lakes. They formed two classes, Chitinivibrionia (high salt- 73 tolerant) and Chitinispirilla (low salt-tolerant) assigned into the phylum Fibrobacteres (Sorokin 74 et al., 2012b; 2016). A single example of an anaerobic proteolytic natronophile isolated from 75 soda lake decaying phototrophic biomass, Proteivorax tanatarense (Clostridiales), has been 76 recently published (Kevbrin et al., 2013). 77 Very few examples of aerobic hydrolytic haloalkaliphiles have been characterized from 78 soda lakes, with most of the work done on alkaline protease producers. The low to moderately 79 salt-tolerant organisms are represented by a well-studied salt-tolerant gammaproteobacterium 80 Alkalimonas amylolytica producing amylase (Ma et al., 2004), Alkalibacillus sp. (Firmicutes), 81 Nesterenkonia sp. (Actinobacteria) and Salinivibrio sp. (Gammaproteobacteria) producing 82 haloalkalitolerant serine proteases (Abdel-Hamed et al., 2016; Gessesse et al., 2003; Lama et al, 83 2005), gammaproteobacteria from the genus Marinimicrobium and actinobacteria utilizing chitin 84 (Sorokin et al., 2012b). 85 Furthermore, a unique group of aerobic extremely halo(natronophilic) hydrolytic 86 Euryarchaeota is also present in hypersaline soda lakes. The previous findings characterized 87 highly haloalkalistable protease-producing Natronococcus occultus, Natrialba magadii, 88 Natronolimnobius innermongolicus (Studdert et al., 2001; de Castro et al., 2008; Selim et al., 89 2014) and amylolytic Natronococcus amylolyticus (Kobayashi et al., 1992). Recently we also 90 demonstrated a presence of four novel genus-level groups of natronoarchaea in soda lakes 91 capable of growth on insoluble celluloses and chitin (Sorokin et al., 2015). 92 However, another type of mainly aerobic soda habitats, saline alkaline soils, also called 93 soda solonchaks, remains practically unexplored as a potential source of aerobic haloalkaliphilic 94 hydrolytics. These habitats differ significantly from soda lakes in that, in contrast to the mostly 95 anoxic soda lake sediments, soda soils are well aerated and dry during most of the year. Such 96 conditions should favour domination by aerobic spore-forming Firmucutes and Actinobacteria, 97 as has been shown in our recent exploration of bacterial nitrogen fixation in such habitats 98 (Sorokin et al., 2008). Soda solonchaks are located in patches in dry steppe and semi-desert 99 areas, such as south Siberia, north-eastern Mongolia, northern China, Egypt, India, Pakistan, 100 Hungary and North American Steppes. In many cases they are hydromorphic and associated with 101 high-standing saline, alkaline ground waters and often occur in the vicinities of saline alkaline 102 (soda) lakes (Basilevich, 1970; Kondorskaya, 1965). 103 In this paper we describe a previously unexplored culturable diversity of aerobic 104 haloalkalitolerant hydrolytic bacteria recovered from saline alkaline soils of several regions in 105 Central Asia, Africa and North America. 106 107 108 Materials and Methods 109 110 Sample characteristics 111 112 Surface soil samples (0-5 cm depth) were collected into sterile plastic Petri dishes at 5 locations 113 in Central Asia, Egypt and California. Each individual sample
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