Symbiosis modulates gene expression of symbionts, but not coral hosts, under thermal challenge.

Increasing ocean temperatures are causing dysbiosis between coral hosts and their symbionts. Previous work suggests that coral host gene expression responds more strongly to environmental stress compared to their intracellular symbionts; however, the causes and consequences of this phenomenon remain untested. We hypothesized that symbionts are less responsive because hosts modulate symbiont environments to buffer stress. To test this hypothesis, we leveraged the facultative symbiosis between the scleractinian coral Oculina arbuscula and its symbiont Breviolum psygmophilum to characterize gene expression responses of both symbiotic partners in and ex hospite under thermal challenges. To characterize host and in hospite symbiont responses, symbiotic and aposymbiotic O. arbuscula were exposed to three treatments: (1) control (18°C), (2) heat (32°C), and (3) cold (6°C). This experiment was replicated with B. psygmophilum cultured from O. arbuscula to characterize ex hospite symbiont responses. Both thermal challenges elicited classic environmental stress responses (ESRs) in O. arbuscula regardless of symbiotic state, with hosts responding more strongly to cold challenge. Hosts also exhibited stronger responses than in hospite symbionts. In and ex hospite B. psygmophilum both down-regulated gene ontology pathways associated with photosynthesis under thermal challenge; however, ex hospite symbionts exhibited greater gene expression plasticity and differential expression of genes associated with ESRs. Taken together, these findings suggest that O. arbuscula hosts may buffer environments of B. psygmophilum symbionts; however, we outline the future work needed to confirm this hypothesis.

Urbanization and edge effects interact to drive mutualism breakdown and the rise of unstable pathogenic communities in forest soil.

Temperate forests are threatened by urbanization and fragmentation, with over 20% (118,300 km2) of U.S. forest land projected to be subsumed by urban land development. We leveraged a unique, well-characterized urban-to-rural and forest edge-to-interior gradient to identify the combined impact of these two land use changes-urbanization and forest edge creation-on the soil microbial community in native remnant forests. We found evidence of mutualism breakdown between trees and their fungal root mutualists [ectomycorrhizal (ECM) fungi] with urbanization, where ECM fungi colonized fewer tree roots and had less connectivity in soil microbiome networks in urban forests compared to rural forests. However, urbanization did not reduce the relative abundance of ECM fungi in forest soils; instead, forest edges alone led to strong reductions in ECM fungal abundance. At forest edges, ECM fungi were replaced by plant and animal pathogens, as well as copiotrophic, xenobiotic-degrading, and nitrogen-cycling bacteria, including nitrifiers and denitrifiers. Urbanization and forest edges interacted to generate new "suites" of microbes, with urban interior forests harboring highly homogenized microbiomes, while edge forest microbiomes were more heterogeneous and less stable, showing increased vulnerability to low soil moisture. When scaled to the regional level, we found that forest soils are projected to harbor high abundances of fungal pathogens and denitrifying bacteria, even in rural areas, due to the widespread existence of forest edges. Our results highlight the potential for soil microbiome dysfunction-including increased greenhouse gas production-in temperate forest regions that are subsumed by urban expansion, both now and in the future.

Soil microbiome predictability increases with spatial and taxonomic scale.

Soil microorganisms shape ecosystem function, yet it remains an open question whether we can predict the composition of the soil microbiome in places before observing it. Furthermore, it is unclear whether the predictability of microbial life exhibits taxonomic- and spatial-scale dependence, as it does for macrobiological communities. Here, we leverage multiple large-scale soil microbiome surveys to develop predictive models of bacterial and fungal community composition in soil, then test these models against independent soil microbial community surveys from across the continental United States. We find remarkable scale dependence in community predictability. The predictability of bacterial and fungal communities increases with the spatial scale of observation, and fungal predictability increases with taxonomic scale. These patterns suggest that there is an increasing importance of deterministic versus stochastic processes with scale, consistent with findings in plant and animal communities, suggesting a general scaling relationship across biology. Biogeochemical functional groups and high-level taxonomic groups of microorganisms were equally predictable, indicating that traits and taxonomy are both powerful lenses for understanding soil communities. By focusing on out-of-sample prediction, these findings suggest an emerging generality in our understanding of the soil microbiome, and that this understanding is fundamentally scale dependent.