Prokaryotic Communities in the Thalassohaline Tuz Lake, Deep Zone, and Kayacik, Kaldirim and Yavsan Salterns (Turkey) Assessed by 16S Rrna Amplicon Sequencing
Total Page：16
File Type：pdf, Size：1020Kb
microorganisms Article Prokaryotic Communities in the Thalassohaline Tuz Lake, Deep Zone, and Kayacik, Kaldirim and Yavsan Salterns (Turkey) Assessed by 16S rRNA Amplicon Sequencing Can Akpolat 1 , Ana Beatriz Fernández 2 , Pinar Caglayan 1 , Baris Calli 3 , Meral Birbir 1,* and Antonio Ventosa 4,* 1 Department of Biology, Faculty of Arts and Sciences, Marmara University, 34722 Istanbul, Turkey; [email protected] (C.A.); [email protected] (P.C.) 2 Institute for Multidisciplinary Research in Applied Biology-IMAB, Universidad Publica de Navarra, Multilva, 31006 Navarra, Spain; [email protected] 3 Department of Environmental Engineering, Faculty of Engineering, Marmara University, 34722 Istanbul, Turkey; [email protected] 4 Department of Microbiology and Parasitology, Faculty of Pharmacy, University of Sevilla, 41004 Sevilla, Spain * Correspondence: [email protected] (M.B.); [email protected] (A.V.); Tel.: +90-216-777-3200 (M.B.); +34-954-556-765 (A.V.) Abstract: Prokaryotic communities and physico-chemical characteristics of 30 brine samples from the thalassohaline Tuz Lake (Salt Lake), Deep Zone, Kayacik, Kaldirim, and Yavsan salterns (Turkey) were analyzed using 16S rRNA amplicon sequencing and standard methods, respectively. Archaea (98.41% of reads) was found to dominate in these habitats in contrast to the domain Bacteria (1.38% of reads). Representatives of the phylum Euryarchaeota were detected as the most predominant, while 59.48% Citation: Akpolat, C.; Fernández, and 1.32% of reads, respectively, were assigned to 18 archaeal genera, 19 bacterial genera, 10 archaeal A.B.; Caglayan, P.; Calli, B.; Birbir, M.; genera, and one bacterial genus that were determined to be present, with more than 1% sequences in Ventosa, A. Prokaryotic Communities the samples. They were the archaeal genera Haloquadratum, Haloarcula, Halorhabdus, Natronomonas, in the Thalassohaline Tuz Lake, Deep Zone, and Kayacik, Kaldirim and Halosimplex, Halomicrobium, Halorubrum, Halonotius, Halolamina, Halobacterium, and Salinibacter within Yavsan Salterns (Turkey) Assessed by the domain Bacteria. The genera Haloquadratum and Halorhabdus were found in all sampling sites. 16S rRNA Amplicon Sequencing. While Haloquadratum, Haloarcula, and Halorhabdus were the most abundant genera, two uncultured Microorganisms 2021, 9, 1525. https:// Tuz Lake Halobacteria (TLHs) 1 and 2 were detected in high abundance, and an additional uncultured doi.org/10.3390/microorganisms9071525 haloarchaeal TLH-3 was found as a minor abundant uncultured taxon. Their future isolation in pure culture would permit us to expand our knowledge on hypersaline thalassohaline habitats, as well as Academic Editor: Ricardo Amils their ecological role and biomedical and biotechnological potential applications. Received: 20 June 2021 Keywords: Tuz Lake (Salt Lake); thalassohaline lakes; salterns; metagenomics; extremophiles; 16S Accepted: 13 July 2021 rRNA amplicon sequencing; physico-chemical analyses Published: 17 July 2021 Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in 1. Introduction published maps and institutional affil- iations. Hypersaline habitats such as salt lakes, saline soils, solar salterns, hypersaline soda lakes, salt mines, and deep-sea and oil reservoir brines are typical extreme environments in which not only NaCl, but other environmental factors, such as pH, temperature, nutrients, radiation, pressure or presence of heavy metals and other toxic compounds, limit their microbiota [1–8]. Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. Hypersaline aquatic environments are classified as thalassohaline habitats; those This article is an open access article derived from marine origin having relative proportions of salts according to those of distributed under the terms and seawater, and athalassohaline aquatic systems, with salts proportions very different from conditions of the Creative Commons seawater, reflecting their non-marine and very different geological origins [1,2,4]. Most Attribution (CC BY) license (https:// studies on hypersaline lakes have been focused on athalassohaline lakes, such as the creativecommons.org/licenses/by/ Dead Sea, hypersaline and alkaline (soda) lakes in Antarctica, East African lakes such 4.0/). as Lake Magadi and the lakes of Wadi Natrun, in Australia or China, especially in Inner Microorganisms 2021, 9, 1525. https://doi.org/10.3390/microorganisms9071525 https://www.mdpi.com/journal/microorganisms Microorganisms 2021, 9, 1525 2 of 19 Microorganisms 2021, 9, 1525 Sea, hypersaline and alkaline (soda) lakes in Antarctica, East African lakes such as 2Lake of 18 Magadi and the lakes of Wadi Natrun, in Australia or China, especially in Inner Mongolia region, and deep-sea lakes [1,2,8–14]. These environments, which host a wide variety of microorganisms belonging to Archaea and Bacteria, have attracted considerable attention Mongolia region, and deep-sea lakes [1,2,8–14]. These environments, which host a wide in recent years in terms of the microbial diversity and their adaptations to high salt con- variety of microorganisms belonging to Archaea and Bacteria, have attracted considerable centrations, as well as on the biotechnological and industrial applications of these ex- attention in recent years in terms of the microbial diversity and their adaptations to high tremophilic microorganisms [5,15–17]. However, relatively little is known about the pro- salt concentrations, as well as on the biotechnological and industrial applications of these karyotic diversity in thalassohaline lakes, including the hypersaline Tuz Lake and its as- extremophilic microorganisms [5,15–17]. However, relatively little is known about the sociated salterns, in Turkey. prokaryotic diversity in thalassohaline lakes, including the hypersaline Tuz Lake and its The hypersaline Tuz Lake (in Turkish Tuz Gölü), located in the Konya Closed Basin associated salterns, in Turkey. on theThe Central hypersaline Anatolian Tuz Peninsula, Lake (in Turkish is the largest Tuz Gölü), hypersaline located in lake the in Konya Turkey, Closed with Basin a max- on 2 imumthe Central surface Anatolian area of 1665 Peninsula, km [18]. is the It has largest an average hypersaline altitude lake of in 905 Turkey, m and with is surrounded a maximum bysurface the K areaızılırmak of 1665 massif km2 in[18 the]. It east, has Obruk an average Plateau altitude in the of south, 905 m Cihanbeyli and is surrounded Plateau byin the the west,Kızılırmak and the massif Haymana in the Plateau east, Obruk in the Plateau north [19]. in the Tuz south, Lake Cihanbeyli constitutes Plateau the Main in theZone west, (a waterand the body Haymana with a Plateaudepth of in about the north 70 cm [19 in]. Tuzthe Lakespring) constitutes and a separate the Main area Zone of the (a waterlake, designatedbody with aas depth the Deep of about Zone 70 (a cm water in the body spring) with and a depth a separate exceeding area of100 the cm lake, in the designated spring), isas found the Deep in the Zone mid-east (a water part body of the with main a depth area of exceeding the lake 100[20,21]. cm inIn theaddition, spring), on is the found shore in ofthe Tuz mid-east Lake, partthere of are the several main area salterns of the that lake are [20, 21the]. Inmajor addition, source on for the salt shore production of Tuz Lake, in Turkey,there are estimated several salterns to meet that 70% are of the the major salt n sourceeeds of for this salt country production [22,23]. in Turkey, Kayacik estimated saltern, Kaldirimto meet 70%saltern, of the and salt Yavsan needs saltern of this are country located [22 in,23 the]. Kayacikmid-east, saltern, north-east, Kaldirim and western saltern, partsand Yavsanof the lake, saltern respectively are located (Figure in the 1). mid-east, The lake north-east, is a closed and water western basin where parts of the the water lake, partlyrespectively filters (Figureinto the1 ).soil The and lake partly is a closedevapor waterates. The basin lake where is mostly the water fed partlyby underground filters into waterthe soil and and partially partly evaporates. by the small The rivers lake isthat mostly come fed from by undergroundKonya Closed water Basin and and partially Obruk Plateau.by the small In summer, rivers thatmost come of the from incoming Konya st Closedreams dry Basin up and and Obruk do not Plateau.reach the In lake. summer, Due tomost the ofexcessive the incoming evaporation, streams the dry lake up dries and out do almost not reach completely the lake. and Due about to the 30 excessivecm thick saltevaporation, layers are theformed. lake driesThe average out almost salt completelycontent and and density about of 30 the cm lake thick water salt are layers 32.4% are andformed. 2–2.5 The g/cm average3, respectively salt content [24]. andThe densityannual ofaverage the lake temperature water are 32.4% is 12 °C and (1.6 2–2.5 °C in g/cm win-3, terrespectively and 22.2 °C [24 in]. summer, The annual respectively), average temperature and the mean is 12 annual◦C (1.6 precipitation◦C in winter is and 324 22.2 mm/m◦C in2. Tuzsummer, Lake respectively),and the surrounding and the meanarea have annual been precipitation determined is as 324 the mm/m most 2arid. Tuz regions Lake and in Turkey.the surrounding area have been determined as the most arid regions in Turkey. FigureFigure 1. 1. LocationsLocations of of the the sampling sampling sites sites and and 30 30 brine brine samples samples coll collectedected from from Tuz Tuz Lake, Lake, Deep Deep Zone, Zone, and and Kayacik, Kayacik, Kaldirim, Kaldirim, andand Yavsan Yavsan salterns in Turkey. Some pollution load reaches the Tuz Lake from various sources located around the lake, especially sulfate-rich wastewater from a sodium sulfate manufacturing plant in the southwest, and partially treated domestic wastewater discharged into the small creeks Microorganisms 2021, 9, 1525 3 of 18 feeding the lake, and to a lesser extent the metal residue particles of the mining activities and fertilizer and pesticide residues originating from the agricultural activities in the region [19].