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Geomicrobiology Journal Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/ugmb20
HCl-Extractable Metal Profiles Correlate with Bacterial Population Shifts in Metal-Impacted Anoxic Coastal Sediment from the Wet/Dry Tropics a
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Alyssa M. Cornall , Stephen Beyer , Alea Rose , Claire Streten-Joyce , Keith a
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McGuinness , David Parry & Karen Gibb a
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Charles Darwin University, Darwin, Australia
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Australian Institute of Marine Science, Darwin, Australia Accepted author version posted online: 18 Apr 2012.Version of record first published: 08 Nov 2012.
To cite this article: Alyssa M. Cornall, Stephen Beyer, Alea Rose, Claire Streten-Joyce, Keith McGuinness, David Parry & Karen Gibb (2013): HCl-Extractable Metal Profiles Correlate with Bacterial Population Shifts in Metal-Impacted Anoxic Coastal Sediment from the Wet/Dry Tropics, Geomicrobiology Journal, 30:1, 48-60 To link to this article: http://dx.doi.org/10.1080/01490451.2011.653083
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Geomicrobiology Journal (2013) 30, 48–60 C Taylor & Francis Group, LLC Copyright ISSN: 0149-0451 print / 1521-0529 online DOI: 10.1080/01490451.2011.653083
Downloaded by [Australian National University], [Claire Streten-Joyce] at 14:49 13 November 2012
HCl-Extractable Metal Profiles Correlate with Bacterial Population Shifts in Metal-Impacted Anoxic Coastal Sediment from the Wet/Dry Tropics ALYSSA M. CORNALL1, STEPHEN BEYER1, ALEA ROSE1, CLAIRE STRETEN-JOYCE2, KEITH MCGUINNESS1, DAVID PARRY2, and KAREN GIBB1∗ 1
Charles Darwin University, Darwin, Australia Australian Institute of Marine Science, Darwin, Australia
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Received August 2011, Accepted December 2011
Metal impacted, anoxic sediments from five sites at a coastal location in the wet/dry tropics of Australia were sampled during both wet and dry seasons. Metal concentrations in total sediment and porewater, and in potentially bioavailable and bioaccessible fractions, were measured. Pyrosequencing was used to sequence bacterial DNA extracted from the sediment, and the sequence data was used to generate community profiles at each sample site. Changes in bacterial populations between sites reflected changes in the concentrations of 7 metals/metalloids (Al, V, Mo, Ga, Zn, Cd, As), and best correlated with the HCl-extractable fraction of metals. Bacterial community structure was also related to physicochemical factors, such as redox potential and organic carbon. Despite a strong sulphide gradient across the transect, acid-volatile sulphide was not significantly correlated to bacterial community structure. We conclude that the bioaccessible fraction of metals to bacteria is partly comprised of particulates, and porewater alone is not a sufficient model for potential metal impact. [Supplementary materials are available for this article. Go to the publisher’s online edition of Geomicrobiology Journal to view the two supplementary tables.] Keywords: bacteria, sediment, coastal, metals, bioavailability
Introduction Aquatic marine sediments in northern Australia are at risk of exposure to elevated levels of multiple metals, particularly coastal sites close to industrial facilities and urban centres (ACIL Tasman and WorleyParsons 2005; Haynes 2001; Munksgaard and Parry 2002). Many of these sites are monitored regularly for sediment quality, however more biological indicators are required to adequately monitor and manage the effects of environmental changes related to metal exposure (ANZECC/ARMCANZ 2000; van Dam et al. 2008). Bacteria are very sensitive to environmental changes and are promising biological indicators (Altug and Balkis 2009; Ryan et al. 2005). However, the relationship between changes in metal This work was funded and supported by the Australian Research Council, Rio Tinto Alcan, Xstrata Zinc McArthur River Mine, Northern Land Council, Northern Territory Research and Innovation Board and the Northern Territory Government. ∗ Address correspondence to Karen Gibb, Research Institute for the Environment and Livelihoods, School of Environmental and Life Sciences, Charles Darwin University, Ellengowan Drive, Brinkin, Northern Territory 0909, Australia; Email:
[email protected]
concentrations and corresponding changes in the composition of bacterial communities in various marine environments is poorly understood. When dealing with sediment, it is also unclear as to what concentrations of metals the bacteria are actually exposed. Toxic exposure from sediment to benthic organisms such as amphipods and worms has been correlated with the concentration of metals in porewater (Ankley et al. 1994). Porewaters contain the most soluble and bio-active forms of metals and are therefore most easily accessed. There is evidence to suggest, however, that bacteria associate with sediment particles in preference to porewater (Albrechtsen 1994; Gillan and Pernet 2007), and may therefore be exposed to significant levels of metals from insoluble fractions in sediment. The bioaccessible fraction of a metal (also defined as environmentally available) is that which may become bioavailable after modification, either prior to or after the organism has come into contact with it; the bioaccessible fraction also includes the bioavailable fraction (Kalman and Turner 2007; Turner et al. 2008). The bioavailable fraction of a metal is that which has immediate potential for metabolism, elimination or bioaccumulation upon contact or ingestion by an organism. Both the bioavailability and bioaccessibility of a metal depend on its physical and chemical characteristics (US EPA 2004).
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Bioavailability of Marine Sediment Metals to Bacteria Metals in sediments are found, in order of decreasing bioavailability, in the following operationally defined chemical forms: Water soluble (includes free ions) > Loosely bound to particulates/exchangeable (including chlorides) > Carbonates > Oxides > Bound to organic material > Sulfides > Residual including minerals (Iwegbue et al. 2007; Tessier et al. 1979). Micro-organisms readily interact with metals in the first three fractions (Chen 1995; Dell’Anno et al. 2003), yet organisms with an acidic gut (e.g., humans) are potentially exposed to everything up to and including metal sulfides if the sediment is ingested. Metals in these fractions are partially extractable with 1M HCl (Agemian and Chau 1977; Di Toro et al. 1990; Louma and Bryan 1981; Snape et al. 2004). Although the 1M HCl-extractable fraction for any given metal is used as a surrogate for the bioavailable concentration in sediment (ANZECC/ARMCANZ 2000), it may not provide an appropriate estimate of the concentrations to which bacteria are exposed. This is because bacteria are subject to multiple routes and mechanisms of exposure (Chen 1995; Gadd 1990). Metal-containing chemical fractions can be experimentally separated to give an indication of the potential bioavailability and bioaccessibility of metals to micro-organisms present within the sediment. Using such methods, we have analyzed anoxic marine sediments, collected in the wet/dry tropics, which contain a suite of metals, and have measured associations between metal levels and bacterial population shifts. Existing studies suggest that bacteria interact with metals in both dissolved and particulate forms (Epstein and Rossel 1995; Gillan and Pernet 2007), and we predict that our results will indicate similar interactions.
Methods Sediment Sampling Marine sediment samples were obtained from Melville Bay, in the Northern Territory, Australia, using a stainless steel Van Veen sediment grab deployed from a boat. Sampling was conducted over two wet seasons (October to April) and two dry seasons (May to September) between 2008 and 2010. The sampling region is close to a bauxite mine/alumina refinery and experiences substantial commercial and recreational boating activity. Samples up to 10 cm deep were collected in duplicate and the temperature, pH and redox potential of sediments were measured by inserting a probe approximately 4 cm into the sediment at the time of sampling. The range of error for redox readings in the field is ±50 meV. Samples were stored in zip-lock plastic bags and acid-washed polypropylene (PP) centrifuge tubes under anaerobic conditions. Samples were placed on ice for transport and were then stored at 4◦ C or at −20◦ C until analysis. Samples were selected to be as physically similar as possible, along a transect of metal concentrations decreasing from the source of impact. The physical and chemical characteristics of each sample site are listed in Table 1. Particle Size Measurement Wet sediments were passed through a 2-mm stainless steel mesh sieve to remove large particles. The remaining material
49 was then passed through a 63 micron stainless steel mesh sieve and dried in an oven at 60◦ C for 3 days. The two fractions of sediment (2 mm - 0.063 mm and