Regional synchrony in full-scale activated sludge bioreactors due to deterministic microbial community assembly

Abstract

Seasonal community structure and regionally synchronous population dynamics have been observed in natural microbial ecosystems, but have not been well documented in wastewater treatment bioreactors. Few studies of community dynamics in full-scale activated sludge systems facing similar meteorological conditions have been done to compare the importance of deterministic and neutral community assembly mechanisms. We subjected weekly activated sludge samples from six regional full-scale bioreactors at four wastewater treatment plants obtained over 1 year to Illumina sequencing of 16S ribosomal RNA genes, resulting in a library of over 17 million sequences. All samples derived from reactors treating primarily municipal wastewater. Despite variation in operational characteristics and location, communities displayed temporal synchrony at the individual operational taxonomic unit (OTU), broad phylogenetic affiliation and community-wide scale. Bioreactor communities were dominated by 134 abundant and highly regionally synchronized OTU populations that accounted for over 50% of the total reads. Non-core OTUs displayed abundance-dependent population synchrony. Alpha diversity varied by reactor, but showed a highly reproducible and synchronous seasonal fluctuation. Community similarity was dominated by seasonal changes, but individual reactors maintained minor stable differences after 1 year. Finally, the impacts of mass migration driven by direct biomass transfers between reactors was investigated, but had no significant effect on community similarity or diversity in the sink community. Our results show that population dynamics in activated sludge bioreactors are consistent with niche-driven assembly guided by seasonal temperature fluctuations.

Figure 1

Regional OTU synchrony in activated sludge communities. (a) Density plot of regional synchrony for ‘core' OTUs (present in all samples) vs a bootstrap sample of randomly selected OTU time-series pairs. Density plots of synchrony as a function of observed frequency and average abundance are shown in b and c. Most OTUs were relatively rare and uncorrelated between plants, but a small number of frequent OTUs were highly synchronized.

Figure 2

Average abundance of the top 15 most abundant bacterial classes at each time point. Sampling date is shown on the x axis. Black lines represent cutoffs for different seasons starting from Fall 2014. Betaproteobacteria were the most dominant class at all time points, but increased in relative abundance between winter and summer. P-values for classes with significantly different abundance in winter and summer are shown in the legend.

Figure 3

Time series of (a) Shannon and (b) Faith's PD alpha diversity for all six reactors. Data shown are average of all samples taken during each month. Alpha diversity was highest in October and November, and lowest in December and March.

Figure 4

Temporal correlograms of time lag between samples versus dissimilarity (weighted unifrac distance) showing the mean and standard deviation (shaded area) for each week. Colors represent whether the compared samples originate from the same reactor (red circles), different reactors at the same plant (blue squares) or different plants (green triangles). The day of year lag between samples correlated well with weighted unifrac distance (R_pearson= 0.47, P<0.001). A full color version of this figure is available at the ISME journal online.

Figure 5

Principal coordinate analysis of weighted unifrac distances between samples. Colors represent season of origin and lines connect samples taken on consecutive sampling trips.