Brooke B. Osborne

Linking microbial community structure and microbial processes: an empirical and conceptual overview

A major goal of microbial ecology is to identify links between microbial community structure and microbial processes. Although this objective seems straightforward, there are conceptual and methodological challenges to designing studies that explicitly evaluate this link. Here, we analyzed literature documenting structure and process responses to manipulations to determine the frequency of structure-process links and whether experimental approaches and techniques influence link detection. We examined nine journals (published 2009-13) and retained 148 experimental studies measuring microbial community structure and processes. Many qualifying papers (112 of 148) documented structure and process responses, but few (38 of 112 papers) reported statistically testing for a link. Of these tested links, 75% were significant and typically used Spearman or Pearsons correlation analysis (68%). No particular approach for characterizing structure or processes was more likely to produce significant links. Process responses were detected earlier on average than responses in structure or both structure and process. Together, our findings suggest that few publications report statistically testing structure-process links. However, when links are tested for they often occur but share few commonalities in the processes or structures that were linked and the techniques used for measuring them.

Nutrient acquisition, soil phosphorus partitioning and competition among trees in a lowland tropical rain forest

We hypothesized that dinitrogen (N2 )- and non-N2 -fixing tropical trees would have distinct phosphorus (P) acquisition strategies allowing them to exploit different P sources, reducing competition. We measured root phosphatase activity and arbuscular mycorrhizal (AM) colonization among two N2 - and two non-N2 -fixing seedlings, and grew them alone and in competition with different inorganic and organic P forms to assess potential P partitioning. We found an inverse relationship between root phosphatase activity and AM colonization in field-collected seedlings, indicative of a trade-off in P acquisition strategies. This correlated with the predominantly exploited P sources in the seedling experiment: the N2 fixer with high N2 fixation and root phosphatase activity grew best on organic P, whereas the poor N2 fixer and the two non-N2 fixers with high AM colonization grew best on inorganic P. When grown in competition, however, AM colonization, root phosphatase activity and N2 fixation increased in the N2 fixers, allowing them to outcompete the non-N2 fixers regardless of P source. Our results indicate that some tropical trees have the capacity to partition soil P, but this does not eliminate interspecific competition. Rather, enhanced P and N acquisition strategies may increase the competitive ability of N2 fixers relative to non-N2 fixers.

Moisture and temperature controls on nitrification differ among ammonia oxidizer communities from three alpine soil habitats

Climate change is altering the timing and magnitude of biogeochemical fluxes in many highelevation ecosystems. The consequent changes in alpine nitrification rates have the potential to influence ecosystem scale responses. In order to better understand how changing temperature and moisture conditions may influence ammonia oxidizers and nitrification activity, we conducted laboratory incubations on soils collected in a Colorado watershed from three alpine habitats (glacial outwash, talus, and meadow). We found that bacteria, not archaea, dominated all ammonia oxidizer communities. Nitrification increased with moisture in all soils and under all temperature treatments. However, temperature was not correlated with nitrification rates in all soils. Site-specific temperature trends suggest the development of generalist ammonia oxidzer communities in soils with greater in situ temperature fluctuations and specialists in soils with more steady temperature regimes. Rapidly increasing temperatures and changing soil moisture conditions could explain recent observations of increased nitrate production in some alpine soils.

Topographic distributions of emergent trees in tropical forests of the Osa Peninsula, Costa Rica

Tropical rainforests are reservoirs of terrestrial carbon and biodiversity. Large and often emergent trees store disproportionately large amounts of aboveground carbon and greatly influence the structure and functioning of tropical rainforests. Despite their importance, controls on the abundance and distribution of emergent trees are largely unknown across tropical landscapes. Conventional field approaches are limited in their ability to characterize patterns in emergent trees across vast landscapes with varying environmental conditions and floristic composition. Here, we used a high-resolution light detection and ranging (LiDAR) sensor aboard the Carnegie Airborne Observatory Airborne Taxonomic Mapping System (CAO-AToMS) to examine the abundance and distribution of tall emergent tree crowns (ETC) relative to surrounding tree crowns (STC) across the Osa Peninsula, a geologically and topographically diverse region of Costa Rica. The abundance of ETC was clearly influenced by fine-scale topographic variation, with distribution patterns that held across a variety of geologic substrates. Specifically, the density of ETC was much greater on lower slopes and in valleys, compared to upper slopes and ridges. Furthermore, using the CAO high-fidelity imaging spectrometer, ETC had a different spectral signature than that of STC. Most notably, ETC had lower remotely sensed foliar nitrogen than STC, which was verified with an independent field survey of canopy leaf chemistry. The underlying mechanisms to explain the topographic-dependence of ETCs and linkages to canopy N are unknown, and remain an important area of research.

Understanding How Microbiomes Influence the Systems they Inhabit: Insight from Ecosystem Ecology

Translating the ever-increasing wealth of information on microbiomes (environment, host, or built environment) to advance the understanding of system-level processes is proving to be an exceptional research challenge. One reason for this challenge is that relationships between characteristics of microbiomes and the system-level processes they influence are often evaluated in the absence of a robust conceptual framework and reported without elucidating the underlying causal mechanisms. The reliance on correlative approaches limits the potential to expand the inference of a single relationship to additional systems and advance the field. We propose that research focused on how microbiomes influence the systems they inhabit should work within a common framework and target known microbial processes that contribute to the system-level processes of interest. Here we identify three distinct categories of microbiome characteristics (microbial processes, microbial community properties, and microbial membership) and propose a framework to empirically link each of these categories to each other and the broader system level processes they affect. We posit that it is particularly important to distinguish microbial community properties that can be predicted from constituent taxa (community aggregated traits) from and those properties that are currently unable to be predicted from constituent taxa (emergent properties). Existing methods in microbial ecology can be applied to more explicitly elucidate properties within each of these categories and connect these three categories of microbial characteristics with each other. We view this proposed framework, gleaned from a breadth of research on environmental microbiomes and ecosystem processes, as a promising pathway with the potential to advance discovery and understanding across a broad range of microbiome science.The well-documented significance of microorganisms to the function of virtually all ecosystems has led to the assumption that more information on microbiomes will improve our ability to understand and predict system-level processes. Notably, the importance of the microbiome has become increasingly evident in the environmental sciences and in particular ecosystem ecology. However, translating the ever-increasing wealth of information on environmental microbiomes to advance ecosystem science is proving exceptionally challenging. One reason for this challenge is that correlations between microbiomes and the ecosystem processes they influence are often reported without the underlying causal mechanisms. This limits the predictive power of each correlation to the time and place at which it was identified. In this paper, we assess the assumptions and approaches currently used to establish links between environmental microbiomes and the ecosystems they influence, propose a framework to more effectively harness our understanding of microbiomes to advance ecosystem science, and identify key challenges and solutions required to apply the proposed framework. Specifically, we suggest identifying each microbial process that contributes to the ecosystem process of interest a priori. We then suggest linking information on microbial community membership through microbial community properties (such as biomass elemental ratios) to the microbial processes that drive each ecosystem process (e.g. N -mineralization). A key challenge in this framework will be identifying which microbial community properties can be determined from the constituents of the community (community aggregated traits, CATs) and which properties are unable to be predicted from a list of their constituent taxa (emergent properties, EPs). We view this directed approach as a promising pathway to advance our understanding of how microbiomes influence the systems they inhabit.

Understanding how microbiomes influence the systems they inhabit

Translating the ever-increasing wealth of information on microbiomes (environment, host or built environment) to advance our understanding of system-level processes is proving to be an exceptional research challenge. One reason for this challenge is that relationships between characteristics of microbiomes and the system-level processes that they influence are often evaluated in the absence of a robust conceptual framework and reported without elucidating the underlying causal mechanisms. The reliance on correlative approaches limits the potential to expand the inference of a single relationship to additional systems and advance the field. We propose that research focused on how microbiomes influence the systems they inhabit should work within a common framework and target known microbial processes that contribute to the system-level processes of interest. Here, we identify three distinct categories of microbiome characteristics (microbial processes, microbial community properties and microbial membership) and propose a framework to empirically link each of these categories to each other and the broader system-level processes that they affect. We posit that it is particularly important to distinguish microbial community properties that can be predicted using constituent taxa (community-aggregated traits) from those properties that cannot currently be predicted using constituent taxa (emergent properties). Existing methods in microbial ecology can be applied to more explicitly elucidate properties within each of these three categories of microbial characteristics and connect them with each other. We view this proposed framework, gleaned from a breadth of research on environmental microbiomes and ecosystem processes, as a promising pathway with the potential to advance discovery and understanding across a broad range of microbiome science.This Review Article discusses the importance of considering known microbial processes to inform our understanding of the role of microbial communities in ecosystem processes, and a move away from approaches based solely on correlation analyses.