Benjamin A. Sikes

Soil microbes drive the classic plant diversity-productivity pattern

Ecosystem productivity commonly increases asymptotically with plant species diversity, and determining the mechanisms responsible for this well-known pattern is essential to predict potential changes in ecosystem productivity with ongoing species loss. Previous studies attributed the asymptotic diversity-productivity pattern to plant competition and differential resource use (e.g., niche complementarity). Using an analytical model and a series of experiments, we demonstrate theoretically and empirically that host-specific soil microbes can be major determinants of the diversity-productivity relationship in grasslands. In the presence of soil microbes, plant disease decreased with increasing diversity, and productivity increased nearly 500%, primarily because of the strong effect of density-dependent disease on productivity at low diversity. Correspondingly, disease was higher in plants grown in conspecific-trained soils than heterospecific-trained soils (demonstrating host-specificity), and productivity increased and host-specific disease decreased with increasing community diversity, suggesting that disease was the primary cause of reduced productivity in species-poor treatments. In sterilized, microbe-free soils, the increase in productivity with increasing plant species number was markedly lower than the increase measured in the presence of soil microbes, suggesting that niche complementarity was a weaker determinant of the diversity-productivity relationship. Our results demonstrate that soil microbes play an integral role as determinants of the diversity-productivity relationship.

Deciphering the relative contributions of multiple functions within plant-microbe symbioses

For microbial symbioses with plants, such as mycorrhizas, we typically quantify either the net effects of one partner on another or a single function a symbiont provides. However, many microbial symbioses provide multiple functions to plants that vary based on the microbial species or functional group, plant species, and environment. Here we quantified the relative contributions of multiple functions provided by arbuscular mycorrhizal (AM) fungi to symbiont-mediated changes in plant biomass. We used two published data sets, one that measured multiple functions (pathogen protection and nutrient uptake) on a single plant and one that measured a single function (pathogen protection) on multiple plants. Using structural equation modeling, we observed strong variation in the functional pathways by which AM fungi altered plant growth; changes in plant biomass were associated with different functions (and different AM fungal functional groups) for the different plant species. Utilizing this methodology across multiple partners and environments will allow researchers to gauge the relative importance of functions they isolate and, perhaps more importantly, those they did not consider. This baseline information is essential for establishing the specific mechanisms by which microbial symbioses influence plant diversity and to more effectively utilize these organisms in agriculture, restoration and conservation.

When do arbuscular mycorrhizal fungi protect plant roots from pathogens

Arbuscular mycorrhizal (AM) fungi are mainly thought to facilitate phosphorus uptake in plants, but they can also perform several other functions that are equally beneficial. Our recent study sheds light on the factors determining one such function, enhanced plant protection from root pathogens. Root infection by the fungal pathogen Fusarium oxysporum was determined by both plant susceptibility and the ability of an AM fungal partner to suppress the pathogen. The non-susceptible plant species (Allium cepa) had limited F. oxysporum infection even without AM fungi. In contrast, the susceptible plant species (Setaria glauca) was heavily infected and only AM fungi in the family Glomeraceae limited pathogen abundance. Plant susceptibility to pathogens was likely determined by contrasting root architectures between plants, with the simple rooted plant (A. cepa) presenting fewer sites for infection.AM fungal colonization, however, was not limited in the same way in part because plants with fewer, simple roots are more mycorrhizal dependent. Protection only by Glomus species also indicates that whatever the mechanism(s) of this function, it responds to AM fungal families differently. While poor at pathogen protection, AM fungal species in the family Gigasporaceae most benefited the growth of the simple rooted plant species. Our research indicates that plant trait differences, such as root architecture can determine how important each mycorrhizal function is to plant growth but the ability to provide these functions differs among AM fungi.

Mycorrhizal fungal growth responds to soil characteristics, but not host plant identity, during a primary lacustrine dune succession

Soil factors and host plant identity can both affect the growth and functioning of mycorrhizal fungi. Both components change during primary succession, but it is unknown if their relative importance to mycorrhizas also changes. This research tested how soil type and host plant differences among primary successional stages determine the growth and plant effects of arbuscular mycorrhizal (AM) fungal communities. Mycorrhizal fungal community, plant identity, and soil conditions were manipulated among three stages of a lacustrine sand dune successional series in a fully factorial greenhouse experiment. Late succession AM fungi produced more arbuscules and soil hyphae when grown in late succession soils, although the community was from the same narrow phylogenetic group as those in intermediate succession. AM fungal growth did not differ between host species, and plant growth was similarly unaffected by different AM fungal communities. These results indicate that though ecological filtering and/or adaptation of AM fungi occurs during this primary dune succession, it more strongly reflects matching between fungi and soils, rather than interactions between fungi and host plants. Thus, AM fungal performance during this succession may not depend directly on the sequence of plant community succession.

Spatial Heterogeneity in Mycorrhizal Populations and Communities: Scales and Mechanisms

The importance of a spatial context in understanding the ecology and evolution of organisms has become increasingly clear. Although there is a growing awareness of the importance of mycorrhizal fungi in many communities and ecosystems, much of this understanding is based on a spatially homogenized view of these soil fungi. This homogenized approach may limit our understanding of how these organisms interact with plants and other biota in the field. As an attempt to advance a spatial framework for understanding mycorrhizal ecology, we review our current understanding of the spatial structure of communities and populations of ectomycorrhizal and arbuscular mycorrhizal fungi at the scale of landscapes, communities, and individual host root systems. A variety of potential mechanisms such as disturbance, abiotic and biotic dispersal of mycorrhizal propagules, and biotic interactions may be responsible for generating and maintaining this spatial variation of populations and communities, but the links between observed spatial patterns and mechanisms have yet to be formed. Future work assessing the potential functional significance of spatial variation of mycorrhizal fungi for plant communities and ecosystem function, as well as measuring spatial variation in mycorrhizal function, will continue to advance our understanding of the spatial template for mycorrhizal–plant interactions in the field.

Determining a minimum detection threshold in terminal restriction fragment length polymorphism analysis.

Terminal restriction fragment length polymorphism (T-RFLP) analysis is a common technique used to characterize soil microbial diversity. The fidelity of this technique in accurately reporting diversity has not been thoroughly evaluated. Here we determine if rare fungal species can be reliably detected by T-RFLP analysis. Spores from three arbuscular mycorrhizal fungal species were each mixed at a range of concentrations (1%, 10%, 50%, and 100%) with Glomus irregulare to establish a minimum detection threshold. T-RFLP analysis was capable of detecting diagnostic peaks of rare taxa at concentrations as low as 1%. The relative proportion of the target taxa in the sample and DNA concentration influenced peak detection reliability. However, low concentrations produced small, inconsistent electropherogram peaks contributing to difficulty in differentiating true peaks from signal noise. The results of this experiment suggest T-RFLP is a reproducible and high fidelity procedure, which requires careful data interpretation in order to accurately characterize sample diversity.

Method or madness: does OTU delineation bias our perceptions of fungal ecology?

This is the authors manuscript. The definitive version is available at www.newphytologist.com

Internalizing Conservation through Our Own Microbes

This is the peer reviewed version of the following article: BA Sikes (2012) Internalizing Conservation through our own Microbes. Conservation Biology, 26(2): 198. http://dx.doi.org/10.1111/j.1523-1739.2012.01834.x, which has been published in final form at http://doi.org/10.1111/j.1523-1739.2012.01834.x. This article may be used for non-commercial purposes in accordance with Wiley Terms and Conditions for Self-Archiving.

Import volumes and biosecurity interventions shape the arrival rate of fungal pathogens

Global trade and the movement of people accelerate biological invasions by spreading species worldwide. Biosecurity measures seek to allow trade and passenger movements while preventing incursions that could lead to the establishment of unwanted pests, pathogens, and weeds. However, few data exist to evaluate whether changes in trade volumes, passenger arrivals, and biosecurity measures have altered rates of establishment of nonnative species over time. This is particularly true for pathogens, which pose significant risks to animal and plant health and are consequently a major focus of biosecurity efforts but are difficult to detect. Here, we use a database of all known plant pathogen associations recorded in New Zealand to estimate the rate at which new fungal pathogens arrived and established on 131 economically important plant species over the last 133 years. We show that the annual arrival rate of new fungal pathogens increased from 1880 to about 1980 in parallel with increasing import trade volume but subsequently stabilised despite continued rapid growth in import trade and recent rapid increases in international passenger arrivals. Nevertheless, while pathogen arrival rates for crop and pasture species have declined in recent decades, arrival rates have increased for forestry and fruit tree species. These contrasting trends between production sectors reflect differences in biosecurity effort and suggest that targeted biosecurity can slow pathogen arrival and establishment despite increasing trade and international movement of people.