Fiddler crab bioturbation determines consistent changes in bacterial communities across contrasting environmental conditions

Abstract

Ecosystem functions are regulated by compositional and functional traits of bacterial communities, shaped by stochastic and deterministic processes. Biogeographical studies have revealed microbial community taxonomy in a given ecosystem to change alongside varying environmental characteristics. Considering that stable functional traits are essential for community stability, we hypothesize that contrasting environmental conditions affect microbial taxonomy rather than function in a model system, testing this in three geographically distinct mangrove forests subjected to intense animal bioturbation (a shared deterministic force). Using a metabarcoding approach combined with sediment microprofiling and biochemistry, we examined vertical and radial sediment profiles of burrows belonging to the pantropical fiddler crab (subfamily Gelasiminae) in three contrasting mangrove environments across a broad latitudinal range (total samples = 432). Each mangrove was environmentally distinct, reflected in taxonomically different bacterial communities, but communities consistently displayed the same spatial stratification (a halo effect) around the burrow which invariably determined the retention of similar inferred functional community traits independent of the local environment.

Figure 1

Study site variation. (a) Map of study sites: a - Thuwal, b - Farasan, c - Mngazana; (b) Principal coordinates analysis of total bacterial OTU assemblages categorized by site (n = 384); (c) Distance-based redundancy analysis (db-RDA) showing significant biogeochemical drivers of bacterial community composition at each site.

Figure 2

OTU variation amongst sediment fractions. Canonical Analysis of Principal coordinates (CAP) of OTU abundance in surface, subsurface and deep sediment for Thuwal (a), Farasan (b) and Mngazana (c). Canonical Analysis of Principal coordinates (CAP) of the bacterial OTU abundance at each ‘Site’, ‘Depth’ and ‘Fraction’ (d–l). Taxonomy bar charts show the relative contribution of different taxa to overall bacterial community composition in burrow and bulk sediment in Thuwal, Farasan and Mngazana in (m) surface, (n) subsurface and (o) deep sediment.

Figure 3

Co-occurrence network analysis of bacterial OTUs in burrow and bulk sediment. Interaction among OTUs in bulk and burrow sediment at (a,b) Thuwal, (c,d) Farasan and (e,f) Mngazana. Boxplots represent the overall degree of connection (g) and closeness centrality (h) of the nodes of each network. (i–k) Phylum degree of connection in burrow and bulk sediment at each site. In each network, the nodes correspond to the OTUs present and are coloured according to phylum affiliation (>97%).

Figure 4

Sediment microbial activity, oxygen concentration and redox. (a) Fluorescein diacetate analysis. Boxplots with standard error of mean showing amount of Fluorescein produced by microbial activity for each sediment fraction in surface, subsurface and deep sediment at Thuwal (n = 6 for each fraction at each depth level). (b) Oxygen concentration microprofiles and (c) redox microprofiles of Thuwal burrow and bulk sediment along a gradient from the burrow wall to bulk. N = 3 for each replicated distance from burrow wall.

Figure 5

Generalised conceptual model of the burrow halo. The overall effects of the burrow on the sediment environment and bacterial community are displayed on either side of the burrow model. Blue, green and grey represent the surface, subsurface and deep sediment layers, respectively. Within each layer, the dark-shade indicates features of the bacterial community or sediment environment that increase toward the burrow; while the light-shade indicates the increase of these features toward bulk sediment. The mixing of sediment along the burrow funnel due to crab activity is indicted.