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Candidatus Scalindua Sp.,” Is Affected by Salinity

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Candidatus Scalindua Sp.,” Is Affected by Salinity View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Hiroshima University Institutional Repository Microbes Environ. Vol. 30, No. 1, 86-91, 2015 https://www.jstage.jst.go.jp/browse/jsme2 doi:10.1264/jsme2.ME14088 Biomass Yield Effciency of the Marine Anammox Bacterium, “Candidatus Scalindua sp.,” is Affected by Salinity Takanori awaTa1, Tomonori kindaichi2*, noriaTsu ozaki2, and akiyoshi ohashi2 1EcoTopia Science Institute, Nagoya University, Nagoya 464–8603, Japan; and 2Department of Civil and Environmental Engineering, Graduate School of Engineering, Hiroshima University, Higashihiroshima 739–8527, Japan (Received June 16, 2014—Accepted December 12, 2014—Published online February 13, 2015) The growth rate and biomass yield effciency of anaerobic ammonium oxidation (anammox) bacteria are markedly lower than those of most other autotrophic bacteria. Among the anammox bacterial genera, the growth rate and biomass yield of the marine anammox bacterium “Candidatus Scalindua sp.” is still lower than those of other anammox bacteria enriched from freshwater environments. The activity and growth of marine anammox bacteria are generally considered to be affected by the presence of salinity and organic compounds. Therefore, in the present study, the effects of salinity and volatile fatty acids (VFAs) on the anammox activity, inorganic carbon uptake, and biomass yield effciency of “Ca. Scalindua sp.” enriched from the marine sediments of Hiroshima Bay, Japan, were investigated in batch experiments. Differences in VFA concentrations (0–10 mM) were observed under varying salinities (0.5%–4%). Anammox activity was high at 0.5%–3.5% salinity, but was 30% lower at 4% salinity. In addition, carbon uptake was higher at 1.5%–3.5% salinity. The results of the present study clearly demonstrated that the biomass yield effciency of the marine anammox bacterium “Ca. Scalindua sp.” was signifcantly affected by salinity. On the other hand, the presence of VFAs up to 10 mM did not affect anammox activity, carbon uptake, or biomass yield effciency. Key words: anaerobic ammonium oxidation (anammox), “Candidatus Scalindua”, biomass yield effciency, salinity, volatile fatty acids Anaerobic ammonium oxidation (anammox) is a microbi- growth rates have been supported by the following stoichi- ological process in which ammonium is oxidized to dinitro- ometry of the anammox process calculated by considering gen gas under anoxic conditions with nitrite as the electron inorganic carbon fxation to cells (anabolism), as originally acceptor (20, 31, 34). This process is mediated by anammox reported by Strous et al. (30): bacteria belonging to the phylum Planctomycetes (31). + − − + Previous studies demonstrated the ubiquitous distribution of 1 NH4 + 1.32 NO2 + 0.066 HCO3 + 0.13 H − anammox bacteria in artifcial and natural ecosystems such as → 1.02 N2 + 0.26 NO3 + 0.066 CH2O0.5N0.15 + 2.03 H2O wastewater treatment plants, freshwater and marine sediments, and soils (2, 7, 8, 19, 24, 28, 29, 39). A minimum of fve Using a membrane bioreactor, Lotti et al. (17) recently genera of candidate anammox bacteria have been tentatively reported the following recalculated stoichiometry under no proposed in Planctomycetes; i.e., “Candidatus Brocadia,” mass transfer limitations and no growth of non-anammox “Ca. Kuenenia,” “Ca. Scalindua,” “Ca. Anammoxoglobus,” bacteria: and “Ca. Jettenia” (9). “Ca. Scalindua” is primarily found in + − − + marine environments (16, 37), and 16S rRNA gene sequences 1 NH4 + 1.146 NO2 + 0.071 HCO3 + 0.057 H − have revealed that this genus contains taxonomically diverse → 0.986 N2 + 0.161 NO3 + 0.071 CH1.74O0.31N0.20 + 2.002 H2O members, even though only a few have been successfully grown in enrichment cultures to date (12, 14, 21, 36). Among the anammox genera, the growth rate of the marine Detailed, but partial information regarding some of the phys- genera “Ca. Scalindua” is markedly lower than that of the iological characteristics of “Ca. Brocadia,” “Ca. Kuenenia,” freshwater genera. This may be attributed to a lower inorganic and “Ca. Scalindua” are currently available (4, 6, 25, 26, 32), carbon fxation (uptake) rate, leading to a lower biomass yield even though they have not yet been isolated in pure cultures. effciency because the maximum specifc ammonium con- + −1 −1 Anammox bacteria are slow growing bacteria even under sumption rate (65 µmol NH4 [g protein] min ) of “Ca. optimal growth conditions in laboratories with reported dou- Scalindua sp.” (4) is similar to that of freshwater anammox bling times of 11 d for “Ca. Brocadia anammoxidans” (30), bacteria (25, 30, 31). In addition, the biomass yield effciency 8.3–11 d for “Ca. Kuenenia stuttgartiensis” (35), 7 d for “Ca. of “Ca. Scalindua sp.” was determined to be 0.030 at 28°C Brocadia sinica” (25), 14.4 d for “Ca. Scalindua sp.” (4), and 3.5% salinity (4). Therefore, the differences observed in 3.6–5.4 d for anammox bacteria enriched from activated growth characteristics between freshwater and marine anammox sludge and estimated by quantitative PCR (33), and 6–10 d bacteria raise questions regarding the infuence of environ- for anammox bacteria enriched from a freshwater lake sedi- mental factors. 29 ment and estimated by N2 measurements (38). These low We hypothesized that differences in the environmental concentrations of salt and certain organic compounds may * Corresponding author. E-mail: [email protected]; affect the inorganic carbon uptake, biomass yield effciency, Tel: +81–82–424–5718; Fax: +81–82–424–5718. and anammox activity of marine anammox bacteria. Therefore, Salinity Affects Yield of Scalindua sp. 87 the present study was conducted to determine the anammox constructed using the ARB NJ (Felsenstein correction), maximum activity and inorganic carbon uptake of the marine anammox parsimony (Phylip DNAPARS), and maximum likelihood (RAxML) bacterium, “Ca. Scalindua sp.” using batch experiments under methods, which were implemented by the ARB software with a database SSU Ref NR 111 dataset (27). A bootstrap resampling different salinity and volatile fatty acid (VFA) concentra- analysis for 1,000 replicates was conducted to estimate the conf- tions. VFAs are also oxidized by both marine and freshwater dence of the tree topologies. anammox bacteria with nitrate as the electron acceptor (10, 11, 36). This metabolic variety may relate to a survival strat- Fluorescence in situ hybridization egy of anammox bacteria in nutrient-limiting environments. Biomass samples were collected from the upfow column reactor and fxed in 4% paraformaldehyde. FISH was subsequently conducted according to the procedure described by Okabe et al. Materials and Methods (23). The 16S rRNA-targeted oligonucleotide probes used in this study were EUBmix, composed of EUB338 (1), EUB338II, and Biomass samples EUB338III (5), which are specifc for most bacteria; Amx368 (29), Biomass samples were obtained from an upfow column reactor which is specifc for all anammox bacteria; and Sca1129a, specifc inoculated with an anammox bioflm, as previously described (14). for uncultured bacterium husup-a2, and Sca1129b, specifc for the The inoculant anammox bioflm contained two phylogenetically uncultured bacterium husup-a7, which distinguish two phylogeneti- distinct “Ca. Scalindua sp.” operated at 20°C (14); therefore, the cally different “Ca. Scalindua sp.” in the inoculum used in this study reactor was operated at 28°C to dominantly proliferate one species, (14). The probes were labeled with Cy3 or Alexa Flour488 at the 5' as previously described (3, 4). The reactor volume was 920 mL and end. A LSM5 PASCAL model confocal laser-scanning microscope, the hydraulic retention time was set to 4 h. The following slightly equipped with an Ar ion laser (488 nm) and HeNe laser (543 nm; modifed version of the synthetic marine nutrient medium reported Carl Zeiss, Oberkochen, Germany), was used for microscopy. The by Kindaichi et al. (14) was fed into the reactor: 28 g L−1 of an arti- average surface area fraction was determined from at least 24 repre- fcial sea salt, SEALIFE (Marine Tech, Tokyo, Japan), 70 mg-N L−1 sentative laser scanning microscopy projection images using the −1 −1 −1 LSM5 PASCAL software provided by Carl Zeiss (13). of (NH4)2SO4, 70 mg-N L of NaNO2, 500 mg L of KHCO3, 27 mg L −1 −1 of KH2PO4, 300 mg L of MgSO4·7H2O, 180 mg L of CaCl2·2H2O, Batch experiments and 1 mL of trace element solutions I and II, as described by van de Batch experiments were performed to investigate the infuence of Graaf et al. (34). The medium was fushed with N2 gas for 1 h to maintain an anaerobic condition (<0.5 mg L−1 of dissolved oxygen) salinity (0.5%–4%) and VFAs (0–10 mM) on the anammox activity, before the addition of nutrients. inorganic carbon uptake, biomass yield effciency, and VFA oxidation rates of “Ca. Scalindua sp.,” as summarized in Table 1. It Phylogenetic analysis should be noted that the batch experiment under 0% salinity condi- Total DNA was extracted from the upfow column reactor using tions was not performed because of the lack of anammox activity the Fast DNA spin kit for soil (MP Biomedicals, Irvine, CA, USA) observed in a previous study (4). The biomass from the upfow col- according to the manufacturer’s instructions. To construct the clone umn reactor was washed twice in the synthetic marine nutrient library, 16S rRNA gene fragments were amplifed using the medium without ammonium and nitrite and was then suspended in Planctomycetales-specifc primer set of Pla46f (22) and 1390r (40). the synthetic marine nutrient medium containing 7 mM ammonium The PCR conditions were as follows: 4 min of initial denaturation at and nitrite at the volatile suspended solids (VSS) concentration of −1 94°C, followed by 30 cycles of 45 s at 94°C, 50 s at 58°C, and 3 min 1 mg VSS mL . A biomass suspension (4 mL) was dispensed into at 72°C.
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