Anthropogenic vs. natural habitats: Higher microbial biodiversity pays the trade-off of lower connectivity

Abstract

Climate change and anthropogenic disturbances are known to influence soil biodiversity. The objectives of this study were to compare the community composition, species coexistence patterns, and ecological assembly processes of soil microbial communities in a paired setting featuring a natural and an anthropogenic ecosystem facing each other at identical climatic, pedological, and vegetational conditions. A transect gradient from forest to seashore allowed for sampling across different habitats within both sites. The field survey was carried out at two adjacent strips of land within the Po River delta lagoon system (Veneto, Italy) one of which is protected within a natural preserve and the other has been converted for decades into a tourist resort. The anthropogenic pressure interestingly led to an increase in the α-diversity of soil microbes but was accompanied by a reduction in β-diversity. The community assembly mechanisms of microbial communities differentiate in natural and anthropic ecosystems: for bacteria, in natural ecosystems deterministic variables and homogeneous selection play a main role (51.92%), while stochastic dispersal limitation (52.15%) is critical in anthropized ecosystems; for fungi, stochastic dispersal limitation increases from 38.1% to 66.09% passing from natural to anthropized ecosystems. We are on calcareous sandy soils and in more natural ecosystems a variation of topsoil pH favors the deterministic selection of bacterial communities, while a divergence of K availability favors stochastic selection. In more anthropized ecosystems, the deterministic variable selection is influenced by the values of SOC. Microbial networks in the natural system exhibited higher numbers of nodes and network edges, as well as higher averages of path length, weighted degree, clustering coefficient, and density than its equivalent sites in the more anthropically impacted environment. The latter on the other hand presented a stronger modularity. Although the influence of stochastic processes increases in anthropized habitats, niche-based selection also proves to impose constraints on communities. Overall, the functionality of the relationships between groups of microorganisms co-existing in communities appeared more relevant to the concept of functional biodiversity in comparison to the plain number of their different taxa. Fewer but functionally more organized lineages displayed traits underscoring a better use of the resources than higher absolute numbers of taxa when those are not equally interconnected in their habitat exploitation. However, considering that network complexity can have important implications for microbial stability and ecosystem multifunctionality, the extinction of complex ecological interactions in anthropogenic habitats may impair important ecosystem services that soils provide us.

Keywords: Anthropogenic habitat; Co-occurrence pattern; Phylogenetic turnover; Soil biodiversity; Soil microbial community.