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Diazotrophic Bacterioplankton in a Coral Reef Lagoon: Phylogeny, Diel Nitrogenase Expression and Response to Phosphate Enrichment

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Diazotrophic Bacterioplankton in a Coral Reef Lagoon: Phylogeny, Diel Nitrogenase Expression and Response to Phosphate Enrichment The ISME Journal (2007) 1, 78–91 & 2007 International Society for Microbial Ecology All rights reserved 1751-7362/07 $30.00 www.nature.com/ismej ORIGINAL ARTICLE Diazotrophic bacterioplankton in a coral reef lagoon: phylogeny, diel nitrogenase expression and response to phosphate enrichment Ian Hewson, Pia H Moisander, Amanda E Morrison and Jonathan P Zehr Department of Ocean Sciences, University of California Santa Cruz, Santa Cruz, CA, USA We investigated diazotrophic bacterioplankton assemblage composition in the Heron Reef lagoon (Great Barrier Reef, Australia) using culture-independent techniques targeting the nifH fragment of the nitrogenase gene. Seawater was collected at 3 h intervals over a period of 72 h (i.e. over diel as well as tidal cycles). An incubation experiment was also conducted to assess the impact of 3À phosphate (PO4 ) availability on nifH expression patterns. DNA-based nifH libraries contained primarily sequences that were most similar to nifH from sediment, microbial mat and surface- associated microorganisms, with a few sequences that clustered with typical open ocean phylotypes. In contrast to genomic DNA sequences, libraries prepared from gene transcripts (mRNA amplified by reverse transcription-polymerase chain reaction) were entirely cyanobacterial and contained phylotypes similar to those observed in open ocean plankton. The abundance of Trichodesmium and two uncultured cyanobacterial phylotypes from previous studies (group A and group B) were studied by quantitative-polymerase chain reaction in the lagoon samples. These were detected as transcripts, but were not detected in genomic DNA. The gene transcript abundance of 3À these phylotypes demonstrated variability over several diel cycles. The PO4 enrichment experiment 3À had a clearer pattern of gene expression over diel cycles than the lagoon sampling, however PO4 additions did not result in enhanced transcript abundance relative to control incubations. The results suggest that a number of diazotrophs in bacterioplankton of the reef lagoon may originate from sediment, coral or beachrock surfaces, sloughing into plankton with the flooding tide. The presence of typical open ocean phylotype transcripts in lagoon bacterioplankton may indicate that they are an important component of the N cycle of the coral reef. The ISME Journal (2007) 1, 78–91; doi:10.1038/ismej.2007.5 Subject Category: microbial ecology and functional diversity of natural habitats Keywords: diazotroph; nitrogen; nitrogenase; coral; reef; expression Introduction ecosystems has received considerably less attention (Moriarty et al., 1985; Moriarty and Hansen, 1990; Coral reefs are important habitats as hotspots of Capone et al., 1992; Capone, 1996; Wild et al., biological diversity and productivity in the oligo- 2004a, b, 2005). Several studies have demonstrated trophic ocean (Capone, 1996). Tropical coral reefs an enormous diversity of coral-associated bacteria are also among the most threatened marine ecosys- and archaea (Cooney et al., 2002; Rohwer et al., tems because of their susceptibility to elevated 2002; Kellogg, 2004; Wegley et al., 2004), and a surface water temperatures (Hughes et al., 2003; recent study of reef flat sediment bacterial and Pandolfi et al., 2003). Most research in these habitats diazotrophic assemblages demonstrated a large has focused upon the biology of conspicuous large degree of patchiness, indicating that these systems metazoa and coral hobionts (Glynn, 1976, 1991; have high diversity (Hewson and Fuhrman, 2006). Koop et al., 2001; Gardner et al., 2003; Saxby et al., Understanding the ecology of functional groups 2003), whereas the microbial ecology of coral reef of bacterioplankton may help to further resolve nutrient cycling budgets in coral reef ecosystems (Charpy-Roubaud et al., 1990; Charpy, 2001; van Correspondence: Dr I Hewson, Department of Ocean Sciences, Duyl et al., 2006). University of California Santa Cruz, 1156 High Street EMS D446, Diazotrophic prokaryotes play a critical role in Santa Cruz, CA 95064, USA. E-mail: [email protected] marine ecosystems as a source of N in marine food Received 19 December 2006; revised and accepted 21 February webs. Nitrogen fixation is carried out by a diverse 2007 suite of prokaryotes in marine plankton, including Diazotrophic bacterioplankton in a coral reef lagoon I Hewson et al 79 colonial and unicellular cyanobacteria and other inorganic N in coral lagoons is typically higher than eubacteria. Diazotrophic activity in oligotrophic in surrounding waters owing to turbulent mixing on waters supports phytoplankton N demand, and sediment surfaces (Charpy-Roubaud et al., 1990). fixed N rapidly enters food webs (Carpenter and Reef cavities, which are present throughout the coral Romans, 1991). The ecology of diazotrophs has been reef framework, are a source for oxidized nitrogen þ investigated in both coastal and open ocean waters, species (however not for NH4 , possibly due to however there have been no previous reports of nitrification) (van Duyl et al., 2006). Tidal flushing diazotroph phylogeny in coral reef lagoons (RLs). through coral reef framework may thus cause Gene-based approaches have been widely used to enhanced nutrient (including nitrogen) concentra- elucidate the ecology of microorganisms in natural tion in lagoon waters, which may ultimately control systems. In the case of marine bacterioplankton, it planktonic biogeochemical processes. is estimated that approximately 99% of taxa are as This study aimed to determine whether hydro- yet uncultured, including several dominant groups dynamic shifts associated with tidal influence, commonly observed in seawater using culture- together with diel cycling, influence the observed independent techniques (Azam, 1998). Studies patterns in diversity and expression of nitrogenase targeting functional genes have considerably ad- (nifH, nitrogen fixation) genes in coral RLs. Water vanced our understanding of the diversity and column samples were collected at regular time activity of biogeochemical processes in the ocean. intervals and over several tidal cycles, and the Open ocean nitrogen fixation was traditionally phylogeny, abundance and expression patterns of ascribed to large colonial taxa of cyanobacteria diazotrophs studied. A phosphate-enrichment ex- (e.g. Trichodesmium), until studies of expression periment was conducted simultaneously to examine of the nitrogenase gene (nifH) in seawater revealed the relationship between phosphate availability and active nitrogenase expression by other cyanobacteria nitrogen cycling activities. Our results indicate that and bacterioplankton (Zehr et al., 2001). the composition and activity of diazotroph assem- High bacterial growth rates (Moriarty et al., 1985; blages is affected by tidal cycles, and that some Moriarty and Hansen, 1990) and low inorganic diazotrophs are responsive to phosphate availability. nutrient concentrations (Charpy-Roubaud et al., 1990; van Duyl et al., 2006) imply nutrient limita- tion of microorganisms in coral reef waters. Nitrogen Materials and methods limitation of microorganism growth is believed to promote nitrogen fixation by microorganisms in Sampling location coral reef sediments (Capone et al., 1992; Capone, Samples were collected near the Heron Island 1996; Koop et al., 2001) and surfaces (Charpy- Research Station, situated on Heron Reef, Great Roubaud et al., 2001; Charpy-Rouband and Larkum, Barrier Reef, Australia, in January 2006. Samples for 2005). Nitrogen fixation rates have been documen- the diel coral RL study were taken approximately ted in coral reef bacterioplankton associated with 5 m from the high tide mark on the reef flat (total the o10 mm size fraction in two coral RLs (Indian water depth was approximately 50 cm at low tide, Ocean and New Caledonia), equivalent to 20–40% and 2.5 m at high tide) within the gutter zone of the of new production (Charpy, 2005). However, the reef (Figure 1). The samples for the phosphate- supply of nitrogen to lagoons and surrounding enrichment experiment were taken at 1545 from the waters is controlled by reef morphology (Dufour Gutter Region in approximately 50 cm of water (total et al., 2001), and the concentration of organic N and water depth), while the tide was receding. Low Tide Flow 200 m High Tide Flow N Australia Heron Island Sampling Location Reef Cres Heron Channel Heron Reef Flat t Figure 1 Map of sampling locations in the Heron Reef lagoon. The dominant flow directions are indicated during flood and ebb tides. The ISME Journal Diazotrophic bacterioplankton in a coral reef lagoon I Hewson et al 80 Reef lagoon sampling in larger sampling volumes or filter sizes with little Reef lagoon sampling began on 1745 on 2 January PCR inhibition. 2006, and concluded at 0015 on 5 January 2006. RNA samples (both 47 and 25 mm filters) were Samples were collected from the sampling location extracted using the RNEasy kit (Qiagen, Valencia, every 4–6 h using an acid-washed and sample- CA, USA) with the following modifications. After rinsed bucket, which was submerged to collect placing the filter in a microcentrifuge tube contain- water from the current. The water was then poured ing approximately 100 ml, 0.1 mm diameter glass into duplicate 4 liter LDPE cubitainers (Nalgene I- beads (BioSpec Inc., Bartlesville, OH, USA), the Chem, Rockwood, TN, USA), which were trans- filters were amended with 350 ml buffer RLT, and the ported immediately to the laboratory for processing. tubes bead-beaten in a BioSpec beadbeater for 6 min. One cubitainer
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