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Vertical Distribution of Functional Potential and Active Microbial Communities in Meromictic Lake Kivu

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Vertical Distribution of Functional Potential and Active Microbial Communities in Meromictic Lake Kivu Microb Ecol DOI 10.1007/s00248-015-0612-9 MICROBIOLOGY OF AQUATIC SYSTEMS Vertical Distribution of Functional Potential and Active Microbial Communities in Meromictic Lake Kivu Özgul İnceoğlu1 & Marc Llirós2,6 & Sean A. Crowe3 & Tamara García-Armisen 1 & Cedric Morana4 & François Darchambeau5 & Alberto V. Borges5 & Jean-Pierre Descy2 & Pierre Servais1 Received: 4 December 2014 /Accepted: 2 April 2015 # Springer Science+Business Media New York 2015 Abstract The microbial community composition in on operational taxonomic units (OTUs at 0.03 cutoff) level meromictic Lake Kivu, with one of the largest CH4 reservoirs, revealed significant and systematic microbial community was studied using 16S rDNA and ribosomal RNA (rRNA) composition shifts with depth. In the oxic zone, pyrosequencing during the dry and rainy seasons. Highly Actinobacteria were found highly dominant in the bulk com- abundant taxa were shared in a high percentage between bulk munity but not in the metabolically active community. In the (DNA-based) and active (RNA-based) bacterial communities, oxic–anoxic transition zone, highly abundant potentially ac- whereas a high proportion of rare species was detected only in tive Nitrospira and Methylococcales were observed. The co- either an active or bulk community, indicating the existence of occurrence of potentially active sulfur-oxidizing and sulfate- a potentially active rare biosphere and the possible underesti- reducing bacteria in the anoxic zone may suggest the presence mation of diversity detected when using only one nucleic acid of an active yet cryptic sulfur cycle. pool. Most taxa identified as generalists were abundant, and those identified as specialists were more likely to be rare in the Keywords Bacteria . Archaea . Pyrosequencing . Active . bulk community. The overall number of environmental pa- Bulk . qPCR . Network . Abundant and rare . Meromicticlake rameters that could explain the variation was higher for abun- dant taxa in comparison to rare taxa. Clustering analysis based Introduction Electronic supplementary material The online version of this article (doi:10.1007/s00248-015-0612-9) contains supplementary material, Meromictic lakes are good model systems for microbial ecol- which is available to authorized users. ogy research due to the high vertical stability of the water masses and physicochemical gradients (in particular oxygen) * Özgul İnceoğlu that lead to relatively constant stratification of microbial pop- [email protected] ulations [1–3]. Since microbes are key players in biogeochem- ical cycles, investigations on microbial diversity and commu- 1 Ecologie des Systèmes Aquatiques, Université Libre de Bruxelles, nity composition are important to understand the ecological Brussel, Belgium functioning of lakes. Environmental heterogeneity was shown 2 Laboratory of Freshwater Ecology, Université de Namur, to produce community differences in lakes [4, 5]. According Namur, Belgium to Lennon and Jones [6], core community shifts, including 3 Departments of Microbiology and Immunology, and Earth, Ocean, active, dormant, and dead cells, may vary widely along verti- and Atmospheric Sciences, University of British Columbia, cal gradients, contributing to the community dynamics as well Vancouver, Canada as to the maintenance of ecosystem biodiversity and ecosys- 4 Department of Earth and Environmental Sciences, Katholieke tem stability. Currently, high-throughput sequencing technol- Universiteit Leuven, Leuven, Belgium ogy provides an opportunity to detect greater microbial diver- 5 Chemical Oceanography Unit, Université de Liège, Liège, Belgium sity than the one detected by previous techniques [7–9]. It has 6 Present address: Department of Genetics and Microbiology, revealed that the core community is composed of abundant Universitat Autònoma de Barcelona, Bellaterra, Spain and rare taxa that are in continuous exchange based on the Ö. İnceoğlu et al. environmental gradients [10]. However, most recent studies depth of 485 m. Surface waters are considered to be oligotro- were based on bulk community composition (i.e., DNA-based phic with moderate primary production compared to other 16S ribosomal RNA (rRNA) genes) and did not distinguish African lakes [22, 23]. Further details on the hydrology, between functionally active (i.e., RNA-based 16S rRNA physicochemistry, and biology of the lake are published else- genes) or dormant populations [11]. Even though potential where [22–25]. In order to study the microbial communities in biases can be introduced during DNA and RNA extraction, the water column of Lake Kivu, water samples were collected complementary DNA (cDNA) synthesis, and PCR amplification from the upper 100 m of the water column in the North basin [12], parallel comparisons of DNA- and RNA-based pyrose- (off Gisenyi; 29.24° E, −1.72° N). Water samples were col- quencing approaches can help differentiate whether abundant lected during two sampling campaigns during both rainy (RS, taxa are active or whether rare but active taxa exist. In addition, February 2012) and dry seasons (DS, September 2012). Up to stronger evidence on the links between biogeochemical process- 20 discrete depths were sampled along a vertical profile be- es and microbial communities might be obtained if active com- tween 1 and 100 m to cover the whole gradient of oxygen munities are monitored rather than bulk communities [13–16]. concentrations (from oxic to anoxic waters). Water samples Lake Kivu in East Africa is a meromictic lake with a per- for chemical and microbiological analyses were collected manent density stratification separating the oxicmixolimnion using a 7.5-L Niskin bottle and stored in 4-L plastic containers − from a deep anoxic monolimnion rich in dissolved salts, car- for chemical analyses (except for CH4 and HS ) and 2-L bon dioxide (CO2), and methane (CH4)[17]. In spite of the Nalgene plastic bottles for biological analyses. Water samples presence of high amounts of CH4 at the bottom of Lake Kivu, for DNA and RNA extractions were immediately passed the CH4 concentration in the oxic zone is surprisingly low through 5.0-μm pore size filters (ISOPORE, Millipore, MA) compared to other lakes globally, due to intense microbial to remove particulate debris as well as large protozoa. Eluents methane oxidation [18, 19]. The vertical stratification of mi- were then passed through 0.22-μm pore size filters crobial taxa and their potential role in biogeochemical cycles (ISOPORE, Millipore, MA) to retain free-living prokaryotes. in Lake Kivu were recently studied for both archaeal and Filters for DNA extraction were preserved in Lysis Buffer as bacterial counterparts using DNA-based analysis, and impor- previously described [21], whereas filters for RNA extraction tant key players of carbon, nitrogen, and sulfur cycles were were preserved in 300 μLofRNAlater(Ambion)andall identified [20, 21]. Furthermore, evaluation of the effect of stored frozen until further analyses. temporal variations on abundant versus rare taxa in different layers revealed that abundant taxa were more stable between Chemical Analyses Temperature, conductivity, pH, and dis- two sampling times than rare ones, indicating a potentially solved oxygen (DO) vertical depth profiles were measured in higher contribution of rare taxa to biogeochemical processes situ with a YSI 6600 V2 (Yellow Spring Instruments, USA) [20]. Therefore, in the present study, Lake Kivu was investi- multiparametric probe. According to Wright et al. [26], the gated as a model ecosystem by comparative DNA- and RNA- upper 100 m of the water column of Lake Kivu was split into based pyrosequencing of bacterial and archaeal communities three distinct vertical layers: an oxic surface layer (DO> in two different seasons (i) to check if bulk (DNA) and poten- 90 μM), a transition zone (DO between 1 and 90 μM), and tially active (RNA) microbial communities have the same a deep anoxic zone (DO<1 μM; Fig. 1). The concentration of composition through the water column and (ii) to explore if methane (CH4) was measured using the headspace technique rare bulk and potentially active taxa respond to environmental with a gas chromatograph with a flame ionization detector as 2− changes as abundant taxa do in Lake Kivu. Furthermore, the previously described [18]. Samples for NOx and SO4 were abundance of key genes related to the carbon (particulate filtered directly through 0.2-μm pore size cellulose acetate + methane monooxygenase gene (pmoA) and methyl syringe filters. NH4 concentrations were determined using coenzyme-M reductase gene (mcrA)) and nitrogen (ammonia the dichloroisocyanurate-salicylate-nitroprussiate colorimetric − monooxygenase gene (amoA), nitrite reductase gene (nirK) method [27]. NO2 concentrations were determined by the − and nitrous oxide reductase (nosZ)) biogeochemical cycles sulfanilamide coloration method [28]. NO3 concentrations was measured to evaluate the functional potential and their were determined after vanadium reduction to nitrite and quan- response to environmental changes. tified in this form following the nitrite determination proce- 2− dure [28, 29]. SO4 concentrations were measured using ion chromatography. Samples for HS−determination were not fil- Materials and Methods tered but preserved instead with zinc acetate and stored frozen. HS−concentrations were measured spectrophotometrically Study Site and Sampling Meromictic and oligotrophic Lake [30]. The detection limits for these methods were 0.5 nM for + − − Kivu is located between Rwanda and the Democratic
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