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Ammoniaoxidizing Archaea and Nitriteoxidizing Nitrospiras in The

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Ammoniaoxidizing Archaea and Nitriteoxidizing Nitrospiras in The RESEARCH ARTICLE Ammonia-oxidizing archaea and nitrite-oxidizing nitrospiras in the biofilter of a shrimp recirculating aquaculture system Monisha N. Brown1, Aurelio Briones2, James Diana3 & Lutgarde Raskin1 1Department of Civil and Environmental Engineering, University of Michigan, Ann Arbor, MI, USA; 2Plant, Soil & Entomological Sciences Department, University of Idaho, Moscow, ID, USA; and 3School of Natural Resources and the Environment, University of Michigan, Ann Arbor, MI, USA Correspondence: Lutgarde Raskin, Abstract Department of Civil and Environmental Engineering, University of Michigan, Ann This study analysed the nitrifier community in the biofilter of a zero discharge, Arbor, MI 48109, USA. Tel.: recirculating aquaculture system (RAS) for the production of marine shrimp in a +1 734 647 6920; fax: +1 734 763 2275; low density (low ammonium production) system. The ammonia-oxidizing e-mail: [email protected] populations were examined by targeting 16S rRNA and amoA genes of ammonia- oxidizing bacteria (AOB) and archaea (AOA). The nitrite-oxidizing bacteria Received 10 February 2012; revised 5 July (NOB) were investigated by targeting the 16S rRNA gene. Archaeal amoA genes 2012; accepted 5 July 2012. Final version published online 9 August 2012. were more abundant in all compartments of the RAS than bacterial amoA genes. Analysis of bacterial and archaeal amoA gene sequences revealed that most DOI: 10.1111/j.1574-6941.2012.01448.x ammonia oxidizers were related to Nitrosomonas marina and Nitrosopumilus maritimus. The NOB detected were related to Nitrospira marina and Nitrospira Editor: Cindy Nakatsu moscoviensis, and Nitrospira marina-type NOB were more abundant than N. mos- coviensis-type NOB. Water quality and biofilm attachment media played a role in Keywords the competitiveness of AOA over AOB and Nitrospira marina-over N. moscovien- ammonia oxidation; nitrite oxidation; sis-type NOB. Nitrospira; Nitrosopumilus maritimus; shrimp aquaculture; recirculating aquaculture system. has been regarded as the ‘Achilles heel’ of wastewater treat- Introduction ment (Daims et al., 2006). In recirculating aquaculture Recirculating aquaculture systems (RAS) for the produc- settings, the challenges associated with accumulation of tion of marine shrimp are a potentially sustainable alter- ammonia and nitrite are similar to those in the wastewater native to traditional aquaculture systems because RAS treatment field and also include problems with low reduce water requirements and limit the concentration of dissolved oxygen (DO) levels, pH outside the optimal range nutrients discharged to receiving waters. RAS require bio- for nitrifying microorganisms (7.5–8.6) and accumulation logical filters to oxidize toxic ammonia and nitrite, and of trace amounts of toxic sulphides (Joye & Hollibaugh, aeration of the water to remove carbon dioxide and 1995; Masser et al., 1999; Ling & Chen, 2005). increase oxygen concentrations (Ebeling, 2000). Nitrifying Less is known about the sensitivity of AOA to environ- biofilters keep ammonia and nitrite concentrations below mental parameters. Archaeal ammonia monooxygenase toxic levels. For the white shrimp, Litopenaeus vannamei subunit A (amoA) gene has been found to be ubiquitous (Boone), ammonia toxicity levels range from 2.44 to in the environment, including in marine waters, biofilters À 3.95 mg L 1 of total ammonia nitrogen (Lin & Chen, of aquaria, coral reefs, estuaries, wastewater treatment 2001), while nitrite toxicity levels vary between 6.1 and plants, hot springs, sediments and soils (Prosser & Nicol, À 25.7 mg L 1 of nitrite-nitrogen (Lin & Chen, 2003). 2008; Erguder et al., 2009; You et al., 2009). In most Nitrification is a two-step process in which ammonia is studies in which the abundances of archaeal and bacterial oxidized to nitrite by ammonia-oxidizing bacteria (AOB) amoA gene copies were investigated, the archaeal amoA MICROBIOLOGY ECOLOGY MICROBIOLOGY or ammonia-oxidizing archaea (AOA) and nitrite is oxi- outnumbered the bacterial amoA gene copies (Erguder dized to nitrate by nitrite-oxidizing bacteria (NOB). The et al., 2009). The factors that influence this distribution sensitivity of AOB and NOB to a wide variety of environ- are still unclear, but Erguder et al. (2009) proposed that mental factors is well known, so much, so that nitrification AOA might be important ammonia oxidizers in low FEMS Microbiol Ecol 83 (2013) 17–25 ª 2012 Federation of European Microbiological Societies Published by Blackwell Publishing Ltd. All rights reserved 18 M.N. Brown et al. nutrient, low pH and sulphide containing environments. Lester, 1992). Because the facility is located away from Furthermore, Martens-Habbena et al. (2009) have shown the coast, artificial seawater was prepared from a com- that AOA have adapted to survive at low ammonia con- mercial salt solution to fill the system. Water quality in centrations, for example, 0.2 lM, concentrations at which the culture tank was measured on site as follows: ammo- AOB cannot grow. nium, nitrite and nitrate concentrations were measured There are four validly described genera of NOB: Ni- using colorimetric assays using Hach kits, DO and tem- trobacter, Nitrospina, Nitrococcus, Nitrospira, as well as a perature were measured with a YSI model 55 DO meter newly communicated NOB species, ‘Candidatus Nitrotoga (Yellow Springs, OH), salinity was measured using a YSI arctica’ (Bartosch et al., 1999; Alawi et al., 2007). Nitro- model 30 salinity meter and pH was determined with a spira spp. have been found to be the main nitrite oxidiz- Mettler-Toledo SevenGo portable pH meter (Schwerzen- ers in wastewater treatment plants (Juretschko et al., bach, Switzerland). All samples for biomass analysis were 1998; Burrell et al., 1999; Daims et al., 2001, 2006) and placed in sterile Whirl-Pak bags (Nasco, Fort Atkinson, the biofilters of a marine RAS (Keuter et al., 2011) WI), and three replicate samples were collected from each because they are better scavengers for nitrite and oxygen location. Samples were collected using sterile equipment than Nitrobacter spp. (Schramm et al., 1999; Koops & from four locations: the culture tank, the bioballs com- Pommerening-Roser, 2001). Nitrospira spp. have also partment, the oyster shell compartment and sludge from been found in a hot spring (Lebedeva et al., 2011), a the basin beneath the filter tower. All samples were stored marine sponge (Off et al., 2010), and various soils (Bart- on ice during transport to the laboratory and processed osch et al., 2002). An analysis of the publicly available within 24 h. sequences of the Nitrospirae phylum (Daims et al., 2001) revealed that the genus Nitrospira consists of at least four DNA extraction distinct sublineages. Nitrification is important to aquaculture in general, DNA from two replicate samples collected from the four but particularly to zero discharge RAS, in which water RAS compartments was extracted using the following quality (specifically ammonia and nitrite concentrations) procedures: for water samples, each replicate consisted of is maintained by biofiltration. DNA extracted from the pellet obtained after centrifuging The success of these systems depends on stable and 250 mL tank water at 3220 g for 30 min. For the bioball reliable performance of its biofilters. The long-term goal compartment, each replicate consisted of DNA extracted of this work is to understand the nitrogen cycling pro- from the biofilm stripped from two bioballs. Biofilm cesses in zero discharge RAS. In the present study, we (average of 260 mg fresh weight) was stripped by examined the nitrifier community in the biofilter of a immersing each bioball in phosphate-buffered saline marine, zero discharge, indoor, recirculating shrimp mat- [130 mM NaCl, 10 mM sodium phosphate buffer (pH uration system, a type of RAS that was operated for the 7.2)] and manually brushing the surface with an endocer- growth and reproduction of L. vannamei. We evaluated vical brush while sonicating for two minutes using a soni- the identities and abundances of nitrifying bacteria and cator bath (L&R, Kearny, NJ). Each sludge sample archaea and found AOA and nitrospiras to be the domi- (average of 560 mg fresh weight) was obtained by centri- nant nitrifiers. Few studies have characterized both AOA fuging 1 mL of the sample at 5000 g for 10 min. The and nitrite oxidizers in marine systems that allow for pro- oyster shells (average of 260 mg fresh weight) were placed cess control. In addition to their industrial importance, directly into bead-beating tubes used for DNA extraction. such systems may serve as important model systems to DNA was extracted from all biomass samples using the improve our understanding of the ecophysiology of AOA FastDNA Spin Kit for Soil (MP Biomedicals, Solon, OH) and NOB. according to the manufacturer’s protocol. Extracted DNA in each sample was quantified using a NanoDrop ND- 1000 Spectrophotometer (Thermo Scientific, Wilmington, Materials and methods DE). Sample collection PCR amplification Samples were collected from an indoor, zero discharge, marine RAS shrimp farm in Okemos, MI (Supporting Duplicate PCRs for each sample replicate were run for Information, Fig. S1). At the time of sampling, the system each primer set. The primers 8F (Lane, 1991) and 1387R had been run continuously for 3 years with minimal (Marchesi et al., 1998) were used to amplify the bacterial water exchange and stable production, although not at 16S rRNA gene (Briones et al., 2007). The archaeal 16S À intensive levels (> 100 shrimp m 2 culture area; Fast & rRNA gene was amplified with the primer set 109f/934b ª 2012 Federation of European Microbiological Societies FEMS Microbiol Ecol 83 (2013) 17–25 Published by Blackwell Publishing Ltd. All rights reserved AOA and nitrospiras in a recirculating aquaculture system 19 (Grosskopf et al., 1998). PCRs were 50 lL and each reac- nonchimera sequences were classified using the classifica- tion contained 5 lLof109 buffer, 200 lM of each tion tool at the Greengenes website. The archaeal and dNTP, 2 mM MgCl2, 0.2 lM of each primer, 1.25 units bacterial amoA and NOB 16S rRNA gene sequences were of Taq Polymerase (ExTaq DNA polymerase; Takara Bio, aligned using MEGA version 4 (Tamura et al., 2007).
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