Saltwater intrusion history shapes the response of bacterial communities upon rehydration
Introduction
Soil bacterial communities are some of the most plentiful and diverse on the planet with an estimated 2.6 × 1029 cells (Whitman et al., 1998, Lozupone and Knight, 2007). In wetlands and freshwater habitats, soil bacteria contribute greatly to biogeochemical cycling of key nutrients, such as nitrogen, phosphorus, sulfur and methane, and are an important sink for carbon (Fuhrman, 2009). These nutrients are essential to plant growth, and the soil bacterial community has an important role in regulating their availability. However, the composition and function of bacteria can be altered by abiotic changes, such as salinity (Horz et al., 2004, Lozupone and Knight, 2007, Jeffries et al., 2012). Under increased salinity regimes, bacterial communities display increases in carbon cycling and photosynthesis and decreases in phosphate and nitrogen cycling (Jackson and Vallaire, 2009, Jeffries et al., 2012, Cañedo-Argüelles et al., 2014).
Saltwater intrusion (SWI) has a significant effect on freshwater ecosystems (Mulrennan and Woodroffe, 1998, Long et al., 2012). The process involves saltwater moving into freshwater habitats due to a number of complex local features, including tidal influences, low altitude, sea-level rise, rainfall, boat traffic and the impact of feral animals (Mulrennan and Woodroffe, 1998, Petty et al., 2007, Hughes, 2010). This can result in the die-off of dominant vegetation and the loss of suitable habitat for aquatic and terrestrial organisms (Winn et al., 2006, Bowman et al., 2010). Grasses such as Pseudoraphis spinescens and Hymenachne acutigluma, which are a major component of the vegetation on freshwater floodplains, and Melaleuca species will potentially be lost due to SWI (Finlayson, 1991). The debris of these grasses left at the end of the wet season and the leaf litter from the Melaleuca species is rich in nitrogen, phosphorous and potassium and they are important contributors to elemental cycling on the floodplains (Finlayson, 1991, Finlayson et al., 1993). Thus, a loss of these grass and Melaleuca species causes a decrease in available nutrients such as nitrogen. Freshwater vegetation species in Kakadu National Park are predicted to decline at ≈ 3.7 psu (practical salinity units) while mangroves in Northern Australia prefer a moderate salinity range of 16 to 50 psu (Ball, 1998). These findings suggest that following SWI, there will potentially be a period of low vegetation and a decrease in nutrient availability on the floodplains.
The Intergovernmental Panel on Climate Change predictions suggest increases of 17–50 cm by 2030–2070 (Stocker et al., 2013). This rise will amplify the occurrence of SWI in many areas, threatening the ecological function and maintenance of biodiversity in high-value wetlands. Because of the region's low topography, extensive areas in Northern Australia are susceptible to sea level rise (Hughes, 2010). Some areas have already undergone dramatic changes caused by SWI (Mulrennan and Woodroffe, 1998, Petty et al., 2007). On the Lower Mary River floodplains located adjacent to Kakadu National Park, more than 17,000 ha of freshwater habitat have been destroyed due to SWI (Mulrennan and Woodroffe, 1998, Bowman et al., 2010). This example provides a window into potential future impacts that predicted sea level rise scenarios could have on nearby World Heritage-listed Kakadu National Park and its extensive range of Ramsar-listed freshwater habitats.
To investigate the impact of SWI on the soil bacterial community of these wetland systems, we simulated a laboratory-based SWI event on floodplain soils collected from sites with contrasting histories of SWI. Changes in bacterial community function and biogeochemical cycling is often indicated by changes in bacterial community composition (Reed and Martiny, 2013). Therefore, bacterial community composition was monitored before and after treatments with saltwater and freshwater.
Section snippets
Study sites
The South Alligator River is located 220 km east of Darwin in the World Heritage-listed Kakadu National Park, Northern Territory, Australia (Fig. 1). It is a macro-tidal river 160 km in length with a tidal range of 5–6 m which extends 105 km up the river (Woodroffe et al., 1989). The floodplains flanking the river were previously covered with mangrove swamps up until 6000 year BP (before present) (Woodroffe et al., 1985, Woodroffe et al., 1989). It was at this time that sea-level stabilised and the
Results and discussion
Replicate samples from sites clustered closely together (Fig. 2). Bacterial community composition of sites with contrasting histories of SWI differed significantly before treatment (PERMANOVA Pairwise Tests: t = 6.84, Pperm ≤ 0.01, Table 1; Fig. 2). Sites with a history of SWI had a greater abundance of OTUs from the genus Desulfobacterium, a known sulfate reducer (Widdell and Bak, 1992) (Fig. 3). Sulfate-reducing bacteria (SRB) respond to higher concentrations of sulfate (SO42 −) (Capone and Kiene,
Acknowledgments
The authors thank the Traditional Owners and Park Rangers from Kakadu National Park who assisted with aspects of the fieldwork. Special thanks for assistance with experimental procedures go to Calista Guthrie. Thanks also to two anonymous reviewers for their valuable comments and criticisms in reviewing this manuscript. This research was financed by the Commonwealth of Australia's National Environmental Research Program with support from the Australian Institute of Marine Science, CSIRO and
References (55)
- et al.
Effects of repeated salt pulses on ecosystem structure and functions in a stream mesocosm
Sci Total Environ
(2014) Production and major nutrient composition of three grass species on the Magela floodplain, Northern territory, Australia
Aquat Bot
(1991)- et al.
Saltwater intrusion into the coastal plains of the Lower Mary River, Northern Territory, Australia
J Environ Manage
(1998) - et al.
Tidal regime, salinity and salt marsh plant zonation
Estuar Coast Shelf Sci
(2005) Permutation tests for univariate or multivariate analysis of variance and regression
Can J Fish Aquat Sci
(2001)Mangrove species richness in relation to salinity and waterlogging: a case study along the Adelaide River floodplain, northern Australia
Glob Ecol Biogeogr Lett
(1998)- et al.
Effects of disturbance intensity and frequency on bacterial community composition and function
PLoS One
(2012) - et al.
Retreating Melaleuca swamp forests in Kakadu National Park: evidence of synergistic effects of climate change and past feral buffalo impacts
Austral Ecol
(2010) - et al.
An ordination of the upland forest communities of Southern Wisconsin
Ecol Monogr
(1957) Summary Statistics Jabiru Airport
(2013)
Comparison of microbial dynamics in marine and freshwater sediments: contrasts in anaerobic carbon catabolism
Limnol Oceanogr
Short-term response of carbon cycling to salinity pulses in a freshwater wetland
Soil Sci Soc Am J
Mechanisms of salinity tolerance in plants
Plant Physiol
Comparison of two next-generation sequencing technologies for resolving highly complex microbiota composition using tandem variable 16S rRNA gene regions
Nucleic Acids Res
PRIMER v 6: user manual/tutorial
Saltwater intrusion and mangrove encroachment of coastal wetlands in the Alligator Rivers Region, Northern Territory, Australia — report 191 supervising scientist, Darwin
Microbial community response to seawater amendment in low-salinity tidal sediments
Microb Ecol
Toward an ecological classification of soil bacteria
Ecology
Influence of drying-rewetting frequency on soil bacterial community structure
Microb Ecol
Biomass and litter dynamics in a Melaleuca forest on a seasonally inundated floodplain in tropical, northern Australia
Wetl Ecol Manag
Soil CO2 flux and photoautotrophic community composition in high-elevation, “barren” soil
Environ Microbiol
Microbial community structure and its functional implications
Nature
Ammonia-oxidizing bacteria respond to multifactorial global change
Proc Natl Acad Sci U S A
Community genomic analyses constrain the distribution of metabolic traits across the Chloroflexi phylum and indicate roles in sediment carbon cycling
Microbiome
Climate change and Australia: key vulnerable regions
Reg Environ Change
R: a language for data analysis and graphics
J Comput Graph Stat
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