Oligotrophic bacteria and pathotrophic fungi moderate multitrophic interactions in semi-arid and arid environments

Future climate projections indicate shifts in intra-annual precipitation patterns, with intensified rainfall events and prolonged dry periods. These changes may alter soil biotic communities and their interactions within food webs, particularly in semi-arid and arid ecosystems. However, the influence of varying rainfall regimes and increasing aridity on multitrophic associations in drylands remains poorly understood.

We leveraged a long-term rainfall manipulation experiment across 6 dryland sites in eastern Australia, including 2 arid ecosystems and 4 semi-arid ecosystems with different levels of rainfall (coefficient of variation, CV), resulting in 3 different climatic conditions. Surface soil was collected from replicated plots subjected to increased (+ 65%) or reduced (- 65%) rainfall relative to ambient conditions using rainout shelter. We characterized bacteria, fungi, protist, and nematode communities using high-throughput amplicon sequencing targeting 16S rRNA, ITS, 18S rRNA and 28S rRNA regions, respectively. Multitrophic co-occurrence network among these groups were constructed to assess biotic responses to rainfall and climatic variations.

Soil biotic community composition in drylands was primarily shaped by environmental conditions, with rainfall treatments exerted no main effect. Belowground multitrophic co-occurrence networks varied significantly across climatic conditions, with aridity promoting positive bacterial associations. Bacteria, fungi, protist formed highly connected modules, and their interactions were central in maintaining multitrophic network structure. Oligotrophic bacteria and pathotrophic fungi emerged as dominant keystone taxa, with their abundance strongly influenced by mean annual precipitation (MAP), underscoring the role of long-term climatic gradients over short-term rainfall changes.

Our findings demonstrate that increasing aridity and rainfall variability reshape soil multitrophic networks in drylands, favoring communities dominated by stress-adapted taxa. The concurrent rise of fungal pathotrophs, potentially driven by declines in protist consumers, may undermine ecosystem resilience. Incorporating multitrophic perspectives into climate impact assessments is essential for anticipating and mitigating emerging threats, such as rising soil-borne pathogens in dryland ecosystems.