Global warming is expected to shift the distributions of plant species and alter plant phenology. While the direct effects of climate change on plants are now readily apparent, determining how climate change affects the interactions between plants and their associated microbiomes is still not resolved. For example, fungal symbionts may not be able to track shifting plant distributions and phenology under future climates. Under this scenario, plants may encounter novel fungal symbionts as their temporal and spatial distributions shift. The consequences of these no-analog plant-fungal symbioses for plants and ecosystem processes are unknown. Here we determine how potential disruption of plant-fungal symbiosis by differential plant and fungal responses to climate change affects both plant productivity and fitness and belowground carbon cycling. We performed a reciprocal transplant experiment of eight different grass species and their belowground fungal symbionts (arbuscular mycorrhizal fungi and root endophytes) between two elevations replicated across three mountainsides near the Rocky Mountain Biological Laboratory. Plants were either grown with their home fungal symbionts, away fungal symbionts, or no symbionts at each elevation. We then measured plant survival, growth rates, and biomass and belowground carbon-degrading enzymes, microbial biomass, and carbon stocks over two years.
Both plants and soils were affected by plant-fungal symbiosis mismatch. Plants grown with home fungi experienced lower mortality and faster growth rates. At the end of two years however, total plant biomass was unaffected by fungal symbiont treatment, suggesting that fungal symbiont effects on plant establishment may be the main consequence of altered plant-fungal symbiosis aboveground. Belowground, soils under plants grown with home fungi had higher activities of carbon-degrading enzymes, which resulted in lower soil carbon stocks at low elevations. Microbial biomass, however, was unaffected by fungal symbiont treatment and instead varied among elevations. This finding suggests that climate may directly affect belowground biomass, but indirect influences of climate via altered plant-fungal symbioses can still change the amount of carbon stored belowground by shifting microbial physiology or composition. These results portend that climate change-induced disruptions to established plant-fungal mutualisms could have long-lasting implications for both plant fitness and belowground carbon storage.