Forfeiting the founder effect: turnover defines biofilm community succession

Abstract

Microbial community succession is a fundamental process that effects underlying functions of almost all ecosystems; yet the roles and fates of the most abundant colonizers are poorly understood. Does early abundance spur long term persistence? How do deterministic and stochastic processes influence the roles of founder species? We performed a succession experiment within a hypersaline microbial mat ecosystem to investigate how ecological processes contributed to the turnover of founder species. Bacterial and micro-eukaryotic founder species were identified from primary succession and tracked through a defined maturation period using 16S and 18S rRNA gene amplicon sequencing in combination with high resolution imaging that utilized stable isotope tracers to evaluate basic functional capabilities. The majority of the founder species did not maintain high relative abundances in later stages of succession.Turnover (versus nestedness) was the dominant process shaping the final community structure. We also asked if different ecological processes acted on bacteria versus eukaryotes during successional stages and found that deterministic and stochastic forces corresponded more with eukaryote and bacterial colonization, respectively. Our results show that taxa from different kingdoms, that share habitat in the tight spatial confines of a biofilm, were influenced by different ecological forces and time scales of succession.

Non‐random processes determine the colonization of groundwater sediments by microbial communities in a pristine porous aquifer

“…This was further reflected by the large dominance of OTU turnover over nestedness between successional stages in the sediment‐attached communities inferred from beta diversity partitioning, showing that the majority of OTUs that had established at a given time point were in fact replaced by others over the course of the succession. Therefore, in agreement with the findings by Brislawn and colleagues (), the mere timing of OTU arrival did not seem to be a determining factor for the final community structure. Rather, the consistent dominance of specific taxa among these persistent OTUs (mainly genera belonging to the Oxalobacteraceae , Comamonadaceae , Caulobacteraceae , Sphingomonadaceae , in addition to Pseudomonas spp.)…”

“…Hence, the total niche space in such microcolonies may be smaller compared with mature biofilms in other environments, similar to what Graham and colleagues () have proposed for sediments in the hyporheic zone. Moreover, although the general pattern of decreasing fractions of newly‐arriving OTUs was also apparent in our experiment, reflecting the saturation of niche space according to Jackson's biofilm model (Jackson, ), we noticed that the fraction of these OTUs at the end of the incubation was still 5–10 times higher compared with findings on biofilms in other environments [e.g., Brislawn and colleagues ()]. These deviations of our results from assembly patterns of biofilms, together with the findings made for hyporheic zone sediments (Graham et al ., ), might point towards important differences in ecological niche structures between biofilms in resource‐rich surface environments and sediment‐attached microbial communities in the typically more energy‐poor and less productive subsurface.…”

“…However, as the biofilm matures further and becomes more heterogeneous, new niches are created that enable specialized species to establish, leading again to an increase in richness and diversity in the mature biofilm. Although Woodcock and Sloan (2017) have demonstrated using a neutral modelling approach that these patterns can be explained based on stochastic processes only, empirical evidence suggests that the assembly of biofilm communities is in fact characterized by a shift from initially stochastic community assembly towards deterministically driven succession at the later stages, for instance caused by species interactions or growing niche space due to increasing spatial and chemical heterogeneity (Martiny et al, 2003;Lyautey et al, 2005;Battin et al, 2016;Veach et al, 2016;Brislawn et al, 2018).…”

“…We used 16S rRNA amplicon sequencing data to study changes in alpha and beta diversity of the sediment-attached communities incubated at the two sites as well as differences in community composition between sediment-attached and planktonic communities in the surrounding groundwater over the course of the succession. To explore the influence of deterministic and stochastic processes on microbial community assembly and succession, we applied the null model approach developed by colleagues (2012, 2013), which has previously also been used in studies on community assembly in the hyporheic zone (Graham et al, 2016b;Stegen et al, 2016a;2018) as well as biofilms in other environments (Langenheder et al, 2017;Brislawn et al, 2018), and thus allows us to compare our results to those previous findings.…”

Selection, Succession, and Stabilization of Soil Microbial Consortia

“…Successional dynamics of soil microbiomes are related to changes in substrate availability and are crucial to predicting ecosystem development (14 – 20). During primary succession, early-colonizing taxa shape available niche space by regulating pH and nutrient availability (16, 17, 21). However, the feedbacks and processes driving successional patterns constitute fundamental knowledge gaps in understanding trajectories of ecosystem development (16, 19).…”