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Abstract
Targeted qPCR and non-targeted amplicon sequencing of 16S rRNA genes within sediment layers identified the anaerobic ammonium oxidation (anammox) niche and characterized microbial community changes attributable to freshwater mussels. Anammox bacteria were normally distributed (Shapiro-Wilk normality test, W-statistic =0.954, p = 0.773) between 1 and 15 cm depth and were increased by a factor of 2.2 (p < 0.001) at 3 cm below the water-sediment interface when mussels were present. Amplicon sequencing of sediment at depths relevant to mussel burrowing (3 and 5 cm) showed that mussel presence reduced observed species richness (p = 0.005), Chao1 diversity (p = 0.005), and Shannon diversity (p < 0.001), with more pronounced decreases at 5 cm depth. A non-metric, multidimensional scaling model showed that intersample microbial species diversity varied as a function of mussel presence, indicating that sediment below mussels harbored distinct microbial communities. Mussel presence corresponded with a 4-fold decrease in a majority of operational taxonomic units (OTUs) classified in the phyla Gemmatimonadetes, Actinobacteria, Acidobacteria, Plantomycetes, Chloroflexi, Firmicutes, Crenarcheota, and Verrucomicrobia. 38 OTUs in the phylum Nitrospirae were differentially abundant (p < 0.001) with mussels, resulting in an overall increase from 25% to 35%. Nitrogen (N)-cycle OTUs significantly impacted by mussels belonged to anammmox genus Candidatus Brocadia, ammonium oxidizing bacteria family Nitrosomonadaceae, ammonium oxidizing archaea genus Candidatus Nitrososphaera, nitrite oxidizing bacteria in genus Nitrospira, and nitrate- and nitrite-dependent anaerobic methane oxidizing organisms in the archaeal family “ANME-2d” and bacterial phylum “NC10”, respectively. Nitrosomonadaceae (0.9-fold (p < 0.001)) increased with mussels, while NC10 (2.1-fold (p < 0.001)), ANME-2d (1.8-fold (p < 0.001)), and Candidatus Nitrososphaera (1.5-fold (p < 0.001)) decreased with mussels. Co-occurrence of 2-fold increases in Candidatus Brocadia and Nitrospira in shallow sediments suggests that mussels may enhance microbial niches at the interface of oxic–anoxic conditions, presumably through biodeposition and burrowing. Furthermore, it is likely that the niches of Candidatus Nitrososphaera and nitrite- and nitrate-dependent anaerobic methane oxidizers were suppressed by mussel biodeposition and sediment aeration, as these phylotypes require low ammonium concentrations and anoxic conditions, respectively. As far as we know, this is the first study to characterize freshwater mussel impacts on microbial diversity and the vertical distribution of N-cycle microorganisms in upper Mississippi river sediment. These findings advance our understanding of ecosystem services provided by mussels and their impact on aquatic biogeochemical N-cycling.
Highlights
Native freshwater mussels (Order Unionida) are ecosystem engineers that significantly alter benthic habitats through biodeposition of feces and pseudofeces, rich in ammonium (NH4+) and organic carbon (C), into sediment (Thorp et al, 1998; Vaughn & Hakenkamp, 2001; Bril et al, 2014)
Our research revealed an increase in anammox bacteria abundance 3 cm below the water-sediment interface when mussels were present, shown for the anammox community using anammox-targeted qPCR (2.2-fold increase) and for Candidatus Brocadia using non-targeted 16S rRNA gene amplicon sequencing (2-fold increase)
In contrast to studies which found significant N-reduction on both a marine mussel (Mytilus californianus) (Pfister, Meyer & Antonopoulos, 2010) and a freshwater mussel (Limnoperna fortunei) (Zhang, Cui & Huang, 2014), our results showed that mussels suppressed n-damo operational taxonomic units (OTUs) in phylum ‘‘NC10’’ (2.1-fold) and family ‘‘ANME-2d’’ (1.8-fold)
Summary
Native freshwater mussels (Order Unionida) are ecosystem engineers that significantly alter benthic habitats through biodeposition of feces and pseudofeces, rich in ammonium (NH4+) and organic carbon (C), into sediment (Thorp et al, 1998; Vaughn & Hakenkamp, 2001; Bril et al, 2014). Mussels live primarily buried in sediment, with their posterior end often flush with the sediment surface (Haag, 2012), or slightly below the surface in soft sediments (Allen & Vaughn, 2009; Allen, 1923; Matteson, 1955) This positions adult freshwater mussels 6–10 cm into the sediment with tendencies toward more shallow burrowing during the spring and summer (Schwalb & Pusch, 2007). That happen to be created by the mussels themselves, are low dissolved oxygen (DO) and elevated ammonia (NH3) and NH4+ (Bril et al, 2017; Haag, 2012) We hypothesize that this frequent vertical and horizontal movement by mussels, many times as an indirect and/or direct response to their own waste production, has a significant impact on porewater chemistry and microbiology in UMR sediments
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