The Origin, Succession, and Predicted Metabolism of Bacterial Communities Associated with Leaf Decomposition.

Intraspecific variation in plant nutrient and defensive traits can regulate ecosystem-level processes, such as decomposition and transformation of plant carbon and nutrients. Understanding the regulatory mechanisms of ecosystem functions at local scales may facilitate predictions of the resistance and resilience of these functions to change. We evaluated how riverine bacterial community assembly and predicted gene content corresponded to decomposition rates of green leaf inputs from red alder trees into rivers of Washington State, USA. Previously, we documented accelerated decomposition rates for leaves originating from trees growing adjacent to the site of decomposition versus more distant locales, suggesting that microbes have a "home-field advantage" in decomposing local leaves. Here, we identified repeatable stages of bacterial succession, each defined by dominant taxa with predicted gene content associated with metabolic pathways relevant to the leaf characteristics and course of decomposition. "Home" leaves contained bacterial communities with distinct functional capacities to degrade aromatic compounds. Given known spatial variation of alder aromatics, this finding helps explain locally accelerated decomposition. Bacterial decomposer communities adjust to intraspecific variation in leaves at spatial scales of less than a kilometer, providing a mechanism for rapid response to changes in resources such as range shifts among plant genotypes. Such rapid responses among bacterial communities in turn may maintain high rates of carbon and nutrient cycling through aquatic ecosystems.IMPORTANCE Community ecologists have traditionally treated individuals within a species as uniform, with individual-level biodiversity rarely considered as a regulator of community and ecosystem function. In our study system, we have documented clear evidence of within-species variation causing local ecosystem adaptation to fluxes across ecosystem boundaries. In this striking pattern of a "home-field advantage," leaves from individual trees tend to decompose most rapidly when immediately adjacent to their parent tree. Here, we merge community ecology experiments with microbiome approaches to describe how bacterial communities adjust to within-species variation in leaves over spatial scales of less than a kilometer. The results show that bacterial community compositional changes facilitate rapid ecosystem responses to environmental change, effectively maintaining high rates of carbon and nutrient cycling through ecosystems

Microbiomes Reduce Their Host's Sensitivity to Interspecific Interactions.

Bacteria associated with eukaryotic hosts can affect host fitness and trophic interactions between eukaryotes, but the extent to which bacteria influence the eukaryotic species interactions within trophic levels that modulate biodiversity and species coexistence is mostly unknown. Here, we used phytoplankton, which are a classic model for evaluating interactions between species, grown with and without associated bacteria to test whether the bacteria alter the strength and type of species interactions within a trophic level. We demonstrate that host-associated bacteria alter host growth rates and carrying capacity. This did not change the type but frequently changed the strength of host interspecific interactions by facilitating host growth in the presence of an established species. These findings indicate that microbiomes can regulate their host species' interspecific interactions. As between-species interaction strength impacts their ability to coexist, our findings show that microbiomes have the potential to modulate eukaryotic species diversity and community composition.IMPORTANCE Description of the Earth's microbiota has recently undergone a phenomenal expansion that has challenged basic assumptions in many areas of biology, including hominid evolution, human gastrointestinal and neurodevelopmental disorders, and plant adaptation to climate change. By using the classic model system of freshwater phytoplankton that has been drawn upon for numerous foundational theories in ecology, we show that microbiomes, by facilitating their host population, can also influence between-species interactions among their eukaryotic hosts. Between-species interactions, including competition for resources, has been a central tenet in the field of ecology because of its implications for the diversity and composition of communities and how this in turn shapes ecosystem functioning

Identifying the plant‐associated microbiome across aquatic and terrestrial environments: the effects of amplification method on taxa discovery

Plants in terrestrial and aquatic environments contain a diverse microbiome. Yet, the chloroplast and mitochondria organelles of the plant eukaryotic cell originate from free‐living cyanobacteria and Rickettsiales. This represents a challenge for sequencing the plant microbiome with universal primers, as ~99% of 16S rRNA sequences may consist of chloroplast and mitochondrial sequences. Peptide nucleic acid clamps offer a potential solution by blocking amplification of host‐associated sequences. We assessed the efficacy of chloroplast and mitochondria‐blocking clamps against a range of microbial taxa from soil, freshwater and marine environments. While we found that the mitochondrial blocking clamps appear to be a robust method for assessing animal‐associated microbiota, Proteobacterial 16S rRNA binds to the chloroplast‐blocking clamp, resulting in a strong sequencing bias against this group. We attribute this bias to a conserved 14‐bp sequence in the Proteobacteria that matches the 17‐bp chloroplast‐blocking clamp sequence. By scanning the Greengenes database, we provide a reference list of nearly 1500 taxa that contain this 14‐bp sequence, including 48 families such as the Rhodobacteraceae, Phyllobacteriaceae, Rhizobiaceae, Kiloniellaceae and Caulobacteraceae. To determine where these taxa are found in nature, we mapped this taxa reference list against the Earth Microbiome Project database. These taxa are abundant in a variety of environments, particularly aquatic and semiaquatic freshwater and marine habitats. To facilitate informed decisions on effective use of organelle‐blocking clamps, we provide a searchable database of microbial taxa in the Greengenes and Silva databases matching various n‐mer oligonucleotides of each PNA sequence.Peer Reviewedhttps://deepblue.lib.umich.edu/bitstream/2027.42/138887/1/men12645.pdfhttps://deepblue.lib.umich.edu/bitstream/2027.42/138887/2/men12645_am.pdfhttps://deepblue.lib.umich.edu/bitstream/2027.42/138887/3/men12645-sup-0001-SupInfo.pd

Genome evolution and host‐microbiome shifts correspond with intraspecific niche divergence within harmful algal bloom‐forming Microcystis aeruginosa

Intraspecific niche divergence is an important driver of species range, population abundance and impacts on ecosystem functions. Genetic changes are the primary focus when studying intraspecific divergence; however, the role of ecological interactions, particularly host‐microbiome symbioses, is receiving increased attention. The relative importance of these evolutionary and ecological mechanisms has seen only limited evaluation. To address this question, we used Microcystis aeruginosa, the globally distributed cyanobacterium that dominates freshwater harmful algal blooms. These blooms have been increasing in occurrence and intensity worldwide, causing major economic and ecological damages. We evaluated 46 isolates of M. aeruginosa and their microbiomes, collected from 14 lakes in Michigan, USA, that vary over 20‐fold in phosphorus levels, the primary limiting nutrient in freshwater systems. Genomes of M. aeruginosa diverged along this phosphorus gradient in genomic architecture and protein functions. Fitness in low‐phosphorus lakes corresponded with additional shifts within M. aeruginosa including genome‐wide reductions in nitrogen use, an expansion of phosphorus assimilation genes and an alternative life history strategy of nonclonal colony formation. In addition to host shifts, despite culturing in common‐garden conditions, host‐microbiomes diverged along the gradient in taxonomy, but converged in function with evidence of metabolic interdependence between the host and its microbiome. Divergence corresponded with a physiological trade‐off between fitness in low‐phosphorus environments and growth rate in phosphorus‐rich conditions. Co‐occurrence of genotypes adapted to different nutrient environments in phosphorus‐rich lakes may have critical implications for understanding how M. aeruginosa blooms persist after initial nutrient depletion. Ultimately, we demonstrate that the intertwined effects of genome evolution, host life history strategy and ecological interactions between a host and its microbiome correspond with an intraspecific niche shift with important implications for whole ecosystem function.Peer Reviewedhttps://deepblue.lib.umich.edu/bitstream/2027.42/151861/1/mec15198_am.pdfhttps://deepblue.lib.umich.edu/bitstream/2027.42/151861/2/mec15198.pdfhttps://deepblue.lib.umich.edu/bitstream/2027.42/151861/3/mec15198-sup-0001-Supinfo.pd

A Taxonomically-informed Mass Spectrometry Search Tool for Microbial Metabolomics Data

MicrobeMASST, a taxonomically-informed mass spectrometry (MS) search tool, tackles limited microbial metabolite annotation in untargeted metabolomics experiments. Leveraging a curated database of >60,000 microbial monocultures, users can search known and unknown MS/MS spectra and link them to their respective microbial producers via MS/MS fragmentation patterns. Identification of microbial-derived metabolites and relative producers, without a priori knowledge, will vastly enhance the understanding of microorganisms’ role in ecology and human health

Diversity of Riparian Plants among and within Species Shapes River Communities

Organismal diversity among and within species may affect ecosystem function with effects transmitting across ecosystem boundaries. Whether recipient communities adjust their composition, in turn, to maximize their function in response to changes in donor composition at these two scales of diversity is unknown. We use small stream communities that rely on riparian subsidies as a model system. We used leaf pack experiments to ask how variation in plants growing beside streams in the Olympic Peninsula of Washington State, USA affects stream communities via leaf subsidies. Leaves from red alder (Alnus rubra), vine maple (Acer cinereus), bigleaf maple (Acer macrophyllum) and western hemlock (Tsuga heterophylla) were assembled in leaf packs to contrast low versus high diversity, and deployed in streams to compare local versus non-local leaf sources at the among and within species scales. Leaves from individuals within species decomposed at varying rates; most notably thin leaves decomposed rapidly. Among deciduous species, vine maple decomposed most rapidly, harbored the least algal abundance, and supported the greatest diversity of aquatic invertebrates, while bigleaf maple was at the opposite extreme for these three metrics. Recipient communities decomposed leaves from local species rapidly: leaves from early successional plants decomposed rapidly in stream reaches surrounded by early successional forest and leaves from later successional plants decomposed rapidly adjacent to later successional forest. The species diversity of leaves inconsistently affected decomposition, algal abundance and invertebrate metrics. Intraspecific diversity of leaf packs also did not affect decomposition or invertebrate diversity. However, locally sourced alder leaves decomposed more rapidly and harbored greater levels of algae than leaves sourced from conspecifics growing in other areas on the Olympic Peninsula, but did not harbor greater aquatic invertebrate diversity. In contrast to alder, local intraspecific differences via decomposition, algal or invertebrate metrics were not observed consistently among maples. These results emphasize that biodiversity of riparian subsidies at the within and across species scale have the potential to affect aquatic ecosystems, although there are complex species-specific effects

Data from: Cascading effects of induced terrestrial plant defenses on aquatic and terrestrial ecosystem function

Herbivores induce plants to undergo diverse processes that minimize costs to the plant, such as producing defences to deter herbivory or reallocating limited resources to inaccessible portions of the plant. Yet most plant tissue is consumed by decomposers, not herbivores, and these defensive processes aimed to deter herbivores may alter plant tissue even after detachment from the plant. All consumers value nutrients, but plants also require these nutrients for primary functions and defensive processes. We experimentally simulated herbivory with and without nutrient additions on red alder (Alnus rubra), which supplies the majority of leaf litter for many rivers in western North America. Simulated herbivory induced a defence response with cascading effects: terrestrial herbivores and aquatic decomposers fed less on leaves from stressed trees. This effect was context dependent: leaves from fertilized-only trees decomposed most rapidly while leaves from fertilized trees receiving the herbivory treatment decomposed least, suggesting plants funnelled a nutritionally valuable resource into enhanced defence. One component of the defence response was a decrease in leaf nitrogen leading to elevated carbon : nitrogen. Aquatic decomposers prefer leaves naturally low in C : N and this altered nutrient profile largely explains the lower rate of aquatic decomposition. Furthermore, terrestrial soil decomposers were unaffected by either treatment but did show a preference for local and nitrogen-rich leaves. Our study illustrates the ecological implications of terrestrial herbivory and these findings demonstrate that the effects of selection caused by terrestrial herbivory in one ecosystem can indirectly shape the structure of other ecosystems through ecological fluxes across boundaries