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Agar-Degrading Bacteria Isolated from Antarctic Macroalgae

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Agar-Degrading Bacteria Isolated from Antarctic Macroalgae Folia Microbiol DOI 10.1007/s12223-017-0511-1 Agar-degrading bacteria isolated from Antarctic macroalgae Roxana Alvarado1 & Sergio Leiva1 Received: 17 May 2016 /Accepted: 23 February 2017 # Institute of Microbiology, Academy of Sciences of the Czech Republic, v.v.i. 2017 Abstract This study describes the taxonomic diversity of Gigartina,andGelidium. The hydrolysis of agar is catalyzed pigmented, agar-degrading bacteria isolated from the surface by agarases which have been classified into three classes of macroalgae collected in King George Island, Antarctica. A based on their mode of action: α-agarase (EC 3.2.1.158), β- total of 30 pigmented, agarolytic bacteria were isolated from agarase (EC 3.2.1.81), and β-porphyranase (EC 3.2.1.–)(Chi the surface of the Antarctic macroalgae Adenocystis et al. 2012). Agarases have potential applications in the food, utricularis, Monostroma hariotii, Iridaea cordata,and cosmetic, and pharmaceutical industries for the production of Pantoneura plocamioides. Based on the 16S rRNA data, the high value-added agaro-oligosaccharides from agar, which agarolytic isolates were affiliated to the genera Algibacter, exhibit various physiological and biological activities (Holdt Arthrobacter, Brachybacterium, Cellulophaga, Citricoccus, and Kraan 2011). Labedella, Microbacterium, Micrococcus, Salinibacterium, Marine bacteria, and in particular those associated with Sanguibacter,andZobellia. Isolates phylogenetically related macroalgae, are a valuable source of novel and exploitable to Cellulophaga algicola showed the highest agarase activity carbohydrate-active enzymes (Michel et al. 2013;Martin in culture supernatants when tested at 4 and 37 °C. This is the et al. 2014). However, only a few studies have explored the first investigation of pigmented agar-degrading bacteria, polysaccharide-degrading activities of Antarctic marine bac- members of microbial communities associated with teria (Tropeano et al. 2012, 2013;Ferrésetal.2015). Antarctic macroalgae, and the results suggest that they repre- Tropeano et al. (2012, 2013) detected amylase, cellulase, sent a potential source of cold-adapted agarases of possible and agarase activities in a diverse group of Antarctic bacteria, biotechnological interest. mainly Gram-negative species, which were isolated from var- ious marine substrates in Potter Cove, King George Island. Marine pigmented heterotrophic bacteria show a wide ge- netic diversity in marine environments, and would play im- Introduction portant roles in the absorption of visible light (Du et al. 2006). However, little information exists on the diversity, ecological Agar is a complex heteropolysaccharide consisting of role, and biotechnological applications of pigmented bacteria agaropectin and agarose, the latter of which is composed of of marine Antarctic environments, especially of those associ- D-galactose and 3,6-anhydro-L-galactose with alternate α- ated with living surfaces. In a recent study, we found a diverse 1,3- and β-1,4-linkages. The main sources of agar are some community of culturable pigmented Gram-positive bacteria red algae, including the genera Porphyra, Gracilaria, associated with marine macroalgae from the King George Island, Antarctica (Leiva et al. 2015). It was shown that rep- resentatives of Agrococcus, Brachybacterium, Citricoccus, and Kocuria exhibited antimicrobial activity against other res- * Sergio Leiva [email protected] ident bacteria. In a study also carried out in King George Island, Vazquez and Mac Cormack (2002) found that nearly 1 Instituto de Bioquímica & Microbiología, Facultad de Ciencias, one-third of the protease-producing bacterial isolates were Universidad Austral de Chile, Casilla, 567 Valdivia, Chile pigmented, mostly yellow and orange colored. Folia Microbiol Antarctic algae have good commercial prospects be- Screening of agarolytic bacteria cause of its chemodiversity, pure, and uncontaminated natural ingredients and probable high content of Pigmented strains were grown in triplicate on a mineral me- phycocolloids (Dhargalkar and Verlecar 2009). The dium containing agar (20 g/L; BD) and Sea Salts (32 g/L; Antarctic marine environment possesses a rich biodiver- SIGMA). After incubation (4 and 20 °C for 10 days), agar sity and high degree of endemism of macroalgal species plates were flooded with Lugol’s stain solution (SIGMA). (Wulff et al. 2009). The Antarctic algal flora is com- The formation of a depression and a clearing zone around posed of 117 species, of which 57 are endemic to the the colony was considered indicative of agar-degrading white continent (Ramírez 2010). Despite this high diver- activity. sity, the bacterial communities associated with Antarctic macroalgae represent a relatively undescribed biological Assay for agarase activity resource. Furthermore, almost nothing is known about their ability to produce biotechologically relevant, agar- Mid-log phase cultures of the agar-degrading strains were in- degrading enzymes. In the present study, diversity of oculated in liquid media containing Sea Salts (32 g/L; pigmented agarolytic bacteria associated with the surface SIGMA), peptone (3 g/L; BD), yeast extract (0.2 g/L; BD), of macroalgae from King George Island was investigat- and a low concentration of melted agar (2 g/L; BD). Cultures ed. In addition, efforts focused on screening for cold- were incubated at 20 °C on a rotary shaker (100 rpm) for 72 h. adapted agarases. Then, cultures were centrifuged (3500g for 10 min at 4 °C), and the cell-free supernatant was used as crude enzyme sus- pension. The enzyme solution was added to phosphate buff- ered saline solution (PBS, pH 7.4) with 0.2% agar and incu- Material and Methods bated at 4 and 37 °C. Agarase activity was determined through the 3,5-dinitrosalicylic acid (DNS) method (Miller 1959), Algal sampling and bacterial isolation which measures the release of reduced sugar equivalents at 540 nm, with D-galactose (SIGMA) as a standard. One unit Macroalgal specimens were collected from different locations of enzymatic activity was defined as the amount of enzyme on King George Island, Antarctic Peninsula in January 2014 required to produce 1 μmol of reducing sugars (measured as (Rodríguez Point, 62° 11′ 57″ S, 58° 56′ 34″ W; Suffield D-galactose) from agar per minute under the condition men- Point, 62° 11′ 47″ S, 58° 55′ 54″ W; Shoa Island, 62° 12′ tioned above. All assays were carried out in triplicate. 12″ S, 58° 56′ 37″ W; Ardley Island, 62° 12′ 35″ S, 58° 55′ 33″ W; Ras Tu; 62° 13′ 17″ S, 58° 53′ 13″ W). Specimens of PCR amplification and sequencing of 16S rRNA genes brown [Adenocystis utricularis (Bory) Skottsberg], green [Monostroma hariotii Gain], and red algae [Iridaea cordata Genomic DNA from agarolytic isolates was extracted using (Turner) Bory, Pantoneura plocamioides Kylin] were col- the GeneJET Genomic DNA Purification kit (Thermo lected as attached plants, placed in individual sterile plas- Scientific). PCR amplifications of 16S rRNA genes were per- tic bags and transported at 4 °C to the laboratory of the formed using the universal primer pair 27F (5′- AGAGTTTG Antarctic research station BBase Prof. Julio Escudero^, ATCMTGGCTCAG -3′ ) and 1492R (5′ -TACG located in Fildes Bay, King George Island. Samples were GYTACCTTGTTACGACTT-3′) and Platinum Taq DNA po- processed immediately after collection for the isolation of lymerase (Invitrogen). PCR was performed in a Mastercycler epiphytic bacteria. Personal (Eppendorf) under the following conditions: initial Algal specimens were rinsed extensively with autoclaved denaturation at 94 °C for 3 min, followed by 30 cycles at and filtered (0.2 μm cellulose acetate filter membranes) nat- 94 °C for 30 s, 55 °C for 30 s, 72 °C for 2 min, and a final ural seawater (AFSW) in order to remove planktonic and extension at 72 °C for 7 min. The amplified products were loosely attached microorganisms. Rinsed samples were purified with a MinElute Gel Extraction kit (QIAGEN), suspendedinAFSW,vigorouslyvortexedfor1min,then and sequenced on a 3130XL Genetic Analyzer (Applied serially diluted in AFSW, and 100 μL of each dilution was Biosystems®) at the Sequencing Unit, Pontificia Universidad plated in triplicate onto Marine Agar 2216 plates (MA, BD) Católica de Chile (Santiago, Chile). The near full-length 16S and seawater agar (SA, 18 g agar, 1 L natural seawater). rRNA gene sequences were compared to those in the da- Plates were incubated at 4 and 20 °C for 2 weeks. tabases GenBank, EMBL, and EzTaxon-e to determine Pigmented colonies were picked based on morphological the nearest bacterial neighbors. Sequence similarities be- characteristics and purified. All pure cultures were examined tween the pigmented isolates and closest relatives were for Gram reaction. Colony pigmentation was determined by determined using the EzTaxon-e server (http://eztaxon-e. using the PerBang color database (http://www.perbang.dk). ezbiocloud.net/) (Kim et al. 2012). Folia Microbiol Sequences were deposited in the NCBI GenBank un- Discussion der accession numbers KR632533–KR632535, KR047773–KR047787, KU896957–KU896972, and It is increasingly clear that alga-associated microbes are a KU925160–KU925167. major resource for the discovery of novel specific enzymes and secondary metabolites (Martin et al. 2014). However, the diversity of epibionts colonizing Antarctic algae is still largely Results unexplored, and their potential biotechnological uses remain to be discovered. Antarctic macroalgae probably possess a In this study, Gram-negative and Gram-positive high content
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