Impact of hydrologic boundaries on microbial planktonic and biofilm communities in shallow terrestrial subsurface environments

Abstract

Subsurface environments contain a large proportion of planetary microbial biomass and harbor diverse communities responsible for mediating biogeochemical cycles important to groundwater used by human society for consumption, irrigation, agriculture and industry. Within the saturated zone, capillary fringe and vadose zones, microorganisms can reside in two distinct phases (planktonic or biofilm), and significant differences in community composition, structure and activity between free-living and attached communities are commonly accepted. However, largely due to sampling constraints and the challenges of working with solid substrata, the contribution of each phase to subsurface processes is largely unresolved. Here, we synthesize current information on the diversity and activity of shallow freshwater subsurface habitats, discuss the challenges associated with sampling planktonic and biofilm communities across spatial, temporal and geological gradients, and discuss how biofilms may be constrained within shallow terrestrial subsurface aquifers. We suggest that merging traditional activity measurements and sequencing/-omics technologies with hydrological parameters important to sediment biofilm assembly and stability will help delineate key system parameters. Ultimately, integration will enhance our understanding of shallow subsurface ecophysiology in terms of bulk-flow through porous media and distinguish the respective activities of sessile microbial communities from more transient planktonic communities to ecosystem service and maintenance.

Figure 1.

Conceptual illustration of representative shallow subsurface environment that includes the vadose, capillary fringe and saturated zones. Arrows depict the movement of water through infiltration, evapotranspiration, capillary rise and re-charge, and the movement of water within and between these zones creates dynamic conditions for the formation and maintenance of subsurface biofilms.

Figure 2.

Conceptual model of subsurface flow and mixing zones and potential effects on biofilm life-cycle dynamics. Subsurface porous media habitats can be conceptually divided into three zones (I, II and III) with respect to ground water flow and mixing. (I) The vadose zone (including the capillary fringe) is variably saturated depending on infiltration episodes and degree of vertical water table fluctuation, (II) Zone II is the ‘shallow’ groundwater zone wherein ground water flow, together with seasonal changes in water table elevation, can cause multi-directional flow (i.e. vertical and horizontal fluctuations) that can result in greater mixing, (III) The ‘deeper’ groundwater zone (zone III) lies below the depth affected by seasonal water table fluctuations. The degree of mixing in zone III is related mainly to the ground water flow field. In zone II the higher level of seasonal mixing could result in a ‘hot spot’ of greater relative biofilm diversity and activity (represented by multi-color sections; biofilm not depicted at scale) (Bougon et al. 2012). Zone I could have lower biofilm diversity/activity due to limited and transient mixing, although it is possible that diversity and activity in zone I would be more similar to zone II than region III. In zone III, which is deeper and has a more consistent ground water flow regime, biofilms would be less diverse/active. The roles of adhesion/detachment/dispersion could vary with the extent of mixing in the different zones and suggests that different mechanisms of microbial community assembly and diversification impact in situ biofilms.