Fine scale functional differences belie taxonomic resilience in a nutrient loaded microbial community

Microbial communities are comprised of a diverse assemblage of taxonomic groups and metabolic functions that carry out important ecosystem processes such as nutrient cycling. The environmental and ecological processes that shape microbial community structure have been of long-standing interest to microbial ecologists.

One context in which the function of microbial communities has important environmental implications is in estuaries, where microbial communities act as an intermediate between human nutrient and pollution runoff and marine systems  This nutrient runoff can have profound implications for fisheries, water quality, and human health (Belkin & Colwell 2006). Thus, the way in which microbial communities respond to nutrient loading has important consequences for better understanding human impacts on ecosystem function and nutrient cycling.

We chose two creeks located in Ipswich, MA, USA for this study, Greenwood and Egypt creek, hereafter referred to as the polluted and reference creeks. Both creeks drain into Plum Island sound and experience tidal fluxes in salinity. The two creeks were located within 5 km of one another, were surrounded by similar salt marsh plant communities and had similar salinity gradients .The Ipswich creek received input from a sewage effluent located near the head of the creek and the reference creek received input water from a local reservoir. We collected metagenomic data from multiple sites along the two creeks and compared our results with studies of microbial community structures based on 16S rDNA amplicon sequencing, in which a single taxonomically informative locus is used to identify the taxonomic composition of a community (Sogin et al. 2006).

Our study identified a clear increase in the abundance of genes involved in the nitrogen cycle in response to nutrient addition from a sewage effluent. In contrast to neutral models, which predict random community assemblage, these results provide clear support for a role of the functional niche that microbes occupy in determining their abundance in sediments. Further, while our work and that of previous studies (Bowen et al. 2011) indicate that taxonomic composition is relatively unchanged under nutrient addition in salt marsh communities, our metagenomic analyses identified a clear difference in the abundance of functional genes related to nutrient metabolism. This discrepancy appears to be due to the fact that similar metabolic functions are often spread among broad taxonomic ranges.

Comparisons of microbial communities among similar environmental samples using 16S amplicon sequencing and functional metagenomics have been met with mixed results, lending support for both neutral and functional responses in communities. Our comparison of microbial communities in salt marsh sediments along a polluted and unpolluted creek reveal a clear role for both processes, with strong functional differences in the abundance of metabolic genes related to nutrient cycling that are spread randomly across a range of functionally redundant taxa.