Bio
Louis joined the Peay lab in 2021 after completing his Ph.D. at the University of South Carolina. His research primarily focuses on the factors that govern the spatial distributions of bacteria and fungi as a function of microbe-microbe and plant-microbe interactions. From genomes to phenomes, Louis fuses both top-down and bottom-up experimental approaches to determine the genetic architecture that undergirds plant microbiome assemblages across landscapes.
All Publications
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Field Reduction of Ectomycorrhizal Fungi Has Cascading Effects on Soil Microbial Communities and Reduces the Abundance of Ectomycorrhizal Symbiotic Bacteria.
Molecular ecology
2024: e17585
Abstract
Specific interactions between bacteria and ectomycorrhizal fungi (EcMF) can benefit plant health, and saprotrophic soil fungi represent a potentially antagonistic guild to these mutualisms. Yet there is little field-derived experimental evidence showing how the relationship among these three organismal groups manifests across time. To bridge this knowledge gap, we experimentally reduced EcMF in forest soils and monitored both bacterial and fungal soil communities over the course of a year. Our analyses demonstrate that soil trenching shifts the community composition of fungal communities towards a greater abundance of taxa with saprotrophic traits, and this shift is linked to a decrease in both EcMF and a common ectomycorrhizal helper bacterial genus, Burkholderia, in a time-dependent manner. These results not only reveal the temporal nature of a widespread tripartite symbiosis between bacteria, EcMF and a shared host tree, but they also refine our understanding of the commonly referenced 'Gadgil effect' by illustrating the cascading effects of EcMF suppression and implicating soil saprotrophic fungi as potential antagonists on bacterial-EcMF interactions.
View details for DOI 10.1111/mec.17585
View details for PubMedID 39524010
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Ectomycorrhizal fungi alter soil food webs and the functional potential of bacterial communities.
mSystems
2024: e0036924
Abstract
Most of Earth's trees rely on critical soil nutrients that ectomycorrhizal fungi (EcMF) liberate and provide, and all of Earth's land plants associate with bacteria that help them survive in nature. Yet, our understanding of how the presence of EcMF modifies soil bacterial communities, soil food webs, and root chemistry requires direct experimental evidence to comprehend the effects that EcMF may generate in the belowground plant microbiome. To this end, we grew Pinus muricata plants in soils that were either inoculated with EcMF and native forest bacterial communities or only native bacterial communities. We then profiled the soil bacterial communities, applied metabolomics and lipidomics, and linked omics data sets to understand how the presence of EcMF modifies belowground biogeochemistry, bacterial community structure, and their functional potential. We found that the presence of EcMF (i) enriches soil bacteria linked to enhanced plant growth in nature, (ii) alters the quantity and composition of lipid and non-lipid soil metabolites, and (iii) modifies plant root chemistry toward pathogen suppression, enzymatic conservation, and reactive oxygen species scavenging. Using this multi-omic approach, we therefore show that this widespread fungal symbiosis may be a common factor for structuring soil food webs.IMPORTANCEUnderstanding how soil microbes interact with one another and their host plant will help us combat the negative effects that climate change has on terrestrial ecosystems. Unfortunately, we lack a clear understanding of how the presence of ectomycorrhizal fungi (EcMF)-one of the most dominant soil microbial groups on Earth-shapes belowground organic resources and the composition of bacterial communities. To address this knowledge gap, we profiled lipid and non-lipid metabolites in soils and plant roots, characterized soil bacterial communities, and compared soils amended either with or without EcMF. Our results show that the presence of EcMF changes soil organic resource availability, impacts the proliferation of different bacterial communities (in terms of both type and potential function), and primes plant root chemistry for pathogen suppression and energy conservation. Our findings therefore provide much-needed insight into how two of the most dominant soil microbial groups interact with one another and with their host plant.
View details for DOI 10.1128/msystems.00369-24
View details for PubMedID 38717159
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A risk assessment framework for the future of forest microbiomes in a changing climate
NATURE CLIMATE CHANGE
2024
View details for DOI 10.1038/s41558-024-02000-7
View details for Web of Science ID 001209541500001
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Co-inoculations of bacteria and mycorrhizal fungi often drive additive plant growth responses.
ISME communications
2024; 4 (1): ycae104
Abstract
Controlled greenhouse studies have shown the numerous ways that soil microbes can impact plant growth and development. However, natural soil communities are highly complex, and plants interact with many bacterial and fungal taxa simultaneously. Due to logistical challenges associated with manipulating more complex microbiome communities, how microbial communities impact emergent patterns of plant growth therefore remains poorly understood. For instance, do the interactions between bacteria and fungi generally yield additive (i.e. sum of their parts) or nonadditive, higher order plant growth responses? Without this information, our ability to accurately predict plant responses to microbial inoculants is weakened. To address these issues, we conducted a meta-analysis to determine the type (additive or higher-order, nonadditive interactions), frequency, direction (positive or negative), and strength that bacteria and mycorrhizal fungi (arbuscular and ectomycorrhizal) have on six phenotypic plant growth responses. Our results demonstrate that co-inoculations of bacteria and mycorrhizal fungi tend to have positive additive effects on many commonly reported plant responses. However, ectomycorrhizal plant shoot height responds positively and nonadditively to co-inoculations of bacteria and ectomycorrhizal fungi, and the strength of additive effects also differs between mycorrhizae type. These findings suggest that inferences from greenhouse studies likely scale to more complex field settings and that inoculating plants with diverse, beneficial microbes is a sound strategy to support plant growth.
View details for DOI 10.1093/ismeco/ycae104
View details for PubMedID 39188310
View details for PubMedCentralID PMC11346365
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Positive interactions between mycorrhizal fungi and bacteria are widespread and benefit plant growth.
Current biology : CB
2023
Abstract
Bacteria, ectomycorrhizal (EcM) fungi, and land plants have been coevolving for nearly 200 million years, and their interactions presumably contribute to the function of terrestrial ecosystems. The direction, stability, and strength of bacteria-EcM fungi interactions across landscapes and across a single plant host, however, remains unclear. Moreover, the genetic mechanisms that govern them have not been addressed. To these ends, we collected soil samples from Bishop pine forests across a climate-latitude gradient spanning coastal California, fractionated the soil samples based on their proximity to EcM-colonized roots, characterized the microbial communities using amplicon sequencing, and generated linear regression models showing the impact that select bacterial taxa have on EcM fungal abundance. In addition, we paired greenhouse experiments with transcriptomic analyses to determine the directionality of these relationships and identify which genes EcM-synergist bacteria express during tripartite symbioses. Our data reveal that ectomycorrhizas (i.e., EcM-colonized roots) enrich conserved bacterial taxa across climatically heterogeneous regions. We also show that phylogenetically diverse EcM synergists are positively associated with plant and fungal growth and have unique gene expression profiles compared with EcM-antagonist bacteria. In sum, we identify common mechanisms that facilitate widespread and diverse multipartite symbioses, which inform our understanding of how plants develop in complex environments.
View details for DOI 10.1016/j.cub.2023.06.010
View details for PubMedID 37369208
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Underground Heroes: Plants and Microbes Partner to Shape Our World
Frontiers for Young Minds
2023
View details for DOI 10.3389/frym.2023.874363
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Examining the genomic features of human and plant-associated Burkholderia strains.
Archives of microbiology
2022; 204 (6): 335
Abstract
Humans and plants have evolved in the near omnipresence of a microbial milieu, and the factors that govern host-microbe interactions continue to require scientific exploration. To better understand if and to what degree patterns between microbial genomic features and host association (i.e., human and plant) exist, I analyzed the genomes of select Burkholderia strains-a bacterial genus comprised of both human and plant-associated strains-that were isolated from either humans or plants. To this end, I uncovered host-specific, genomic patterns related to metabolic pathway potentials in addition to convergent features that may be related to pathogenic overlap between hosts. Together, these findings detail the genomic associations of human and plant-associated Burkholderia strains and provide a framework for future investigations that seek to link host-host transmission potentials.
View details for DOI 10.1007/s00203-022-02953-3
View details for PubMedID 35587294
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Linking Reactive Oxygen Species (ROS) to Abiotic and Biotic Feedbacks in Plant Microbiomes: The Dose Makes the Poison.
International journal of molecular sciences
2022; 23 (8)
Abstract
In nature, plants develop in complex, adaptive environments. Plants must therefore respond efficiently to environmental stressors to maintain homeostasis and enhance their fitness. Although many coordinated processes remain integral for achieving homeostasis and driving plant development, reactive oxygen species (ROS) function as critical, fast-acting orchestrators that link abiotic and biotic responses to plant homeostasis and development. In addition to the suite of enzymatic and non-enzymatic ROS processing pathways that plants possess, they also rely on their microbiota to buffer and maintain the oxidative window needed to balance anabolic and catabolic processes. Strong evidence has been communicated recently that links ROS regulation to the aggregated function(s) of commensal microbiota and plant-growth-promoting microbes. To date, many reports have put forth insightful syntheses that either detail ROS regulation across plant development (independent of plant microbiota) or examine abiotic-biotic feedbacks in plant microbiomes (independent of clear emphases on ROS regulation). Here we provide a novel synthesis that incorporates recent findings regarding ROS and plant development in the context of both microbiota regulation and plant-associated microbes. Specifically, we discuss various roles of ROS across plant development to strengthen the links between plant microbiome functioning and ROS regulation for both basic and applied research aims.
View details for DOI 10.3390/ijms23084402
View details for PubMedID 35457220
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The genus Caulobacter and its role in plant microbiomes.
World journal of microbiology & biotechnology
1800; 38 (3): 43
Abstract
Recent omics approaches have revealed the prevalent microbial taxa that constitute the microbiome of various plant species. Across global scales and environmental conditions, strains belonging to the bacterial genus Caulobacter have consistently been found in association with various plant species. Aligned with agroecological relevance and biotechnological advances, many scientific communications have demonstrated that several Caulobacter strains (spanning several Caulobacter species) harbor the potential to enhance plant biomass for various plant species ranging from Arabidopsis to Citrullus and Zea mays. In the past several years, co-occurrence data have driven mechanistically resolved communications about select Caulobacter-plant interactions. Given the long-standing history of Caulobacter as a model organism for cell cycle regulation, genetic studies, and the prevalence of Caulobacter species in various plant microbiomes, the genus Caulobacter offers researchers a unique opportunity to leverage for investigating plant-microbe interactions and realizing targeted biotechnological applications. In this review, recent developments regarding Caulobacter-plant interactions are presented in terms of model utility for future biotechnological investigations.
View details for DOI 10.1007/s11274-022-03237-0
View details for PubMedID 35064419
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S2B, a Temperate Bacteriophage That Infects Caulobacter Crescentus Strain CB15.
Current microbiology
2022; 79 (4): 98
Abstract
The Caulobacter crescentus strain CB15 has been the basis of numerous studies designed to characterize the biphasic life cycle of this bacterium. Here we describe a newly isolated podovirus, designated S2B, which is capable of integrating into the CB15 chromosome by recombining with the 3'-end of a particular tRNA-ser gene. In addition, we show that S2B is a representative of a family of closely related prophages that are present in the genomes of characterized strains from several Alphaproteobacteria genera. In contrast, only distantly related bacteriophage genomes are present in the GenBank database. The 42,846 bp S2B genome includes 262 bp terminal repeats, and it contains 62 genes of which 45 code for proteins of unknown function. Proteins with predicted functions include a T7 DNA polymerase, a T3/T7 RNA polymerase, and a T7 helicase/primase suggesting that S2B is part of the Studiervirinae subfamily of the Autographiviridae family.
View details for DOI 10.1007/s00284-022-02799-4
View details for PubMedID 35150327
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Plant-growth-promoting Caulobacter strains isolated from distinct plant hosts share conserved genetic factors involved in beneficial plant-bacteria interactions.
Archives of microbiology
1800; 204 (1): 43
Abstract
The genus Caulobacter encompasses several strains that can enhance the biomass of several plant species. However, for many plant-growth-promoting (PGP) Caulobacter strains, their genomic factors that facilitate positive interactions with their plant hosts remain unknown. Given that leveraging comparative genomics analyses can establish a framework to understand these plant-bacteria interactions, the genomes of three PGP Caulobacter strains that were isolated from distinct geographical locations and have been shown to associate with distinct plant species were compared. Using previously reported analyses to contextualize the genomic patterns among PGP Caulobacter strains, each of these PGP Caulobacter strains (CBR1, RHG1, and RHGG3) was observed harboring similar metabolic potentials and previously reported PGP genetic factors in their genomes. Together, these findings reinforce previous analyses that identify the cyo operon as a general PGP factor for Caulobacter strains while establishing a framework for further investigations that seek to uncover the mechanistic details that govern interactions between Caulobacter strains and diverse plant species.
View details for DOI 10.1007/s00203-021-02702-y
View details for PubMedID 34932160
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Complete Genome Sequence of the Plant-Growth-Promoting Bacterium Caulobacter segnis CBR1
CURRENT MICROBIOLOGY
2021; 78 (8): 2935-2942
Abstract
Genomic sequencing has vastly expedited our understanding of bacterial functions. However, the genomes of many plant-growth-promoting bacteria (PGPB) have yet to be sequenced and contextualized. To this end, I report the sequenced genome of a PGPB-Caulobacter segnis CBR1-and contextualize its genomic features with the genomic features of sequenced Caulobacter strains. Moreover, I demonstrate that the CBR1 genome harbors genomic features that have been shown to be necessary for select Caulobacter strains to enhance the growth and development of Arabidopsis plants. Together, these findings will help guide future investigations that seek to understand the molecular factors undergirding the positive interactions between plants and microbes.
View details for DOI 10.1007/s00284-021-02548-z
View details for Web of Science ID 000655889800002
View details for PubMedID 34047832
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Genes related to redox and cell curvature facilitate interactions between Caulobacter strains and Arabidopsis
PLOS ONE
2021; 16 (4): e0249227
Abstract
Bacteria play an integral role in shaping plant growth and development. However, the genetic factors that facilitate plant-bacteria interactions remain largely unknown. Here, we demonstrated the importance of two bacterial genetic factors that facilitate the interactions between plant-growth-promoting (PGP) bacteria in the genus Caulobacter and the host plant Arabidopsis. Using homologous recombination, we disrupted the cytochrome ubiquinol oxidase (cyo) operon in both C. vibrioides CB13 and C. segnis TK0059 by knocking out the expression of cyoB (critical subunit of the cyo operon) and showed that the mutant strains were unable to enhance the growth of Arabidopsis. In addition, disruption of the cyo operon, metabolomic reconstructions, and pH measurements suggested that both elevated cyoB expression and acid production by strain CB13 contribute to the previously observed inhibition of Arabidopsis seed germination. We also showed that the crescent shape of the PGP bacterial strain C. crescentus CB15 contributes to its ability to enhance plant growth. Thus, we have identified specific genetic factors that explain how select Caulobacter strains interact with Arabidopsis plants.
View details for DOI 10.1371/journal.pone.0249227
View details for Web of Science ID 000636467000036
View details for PubMedID 33793620
View details for PubMedCentralID PMC8016251
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NovelCaulobacterbacteriophages illustrate the diversity of the podovirus genusRauchvirus
ARCHIVES OF VIROLOGY
2020; 165 (11): 2549-2554
Abstract
The podovirus BPP-1 is currently the only member of the Podovirus genus Rauchvirus. Here, we describe three new Caulobacter bacteriophages (Jess A, SR18, and RW) that show genetic similarity to BPP-1 but have many different genetic and structural features that differentiate them from BPP-1. Jess A and SR18 are closely related to each other and should be considered two members of a new species. They share a similar gene order with BPP-1. However, they do not appear to form lysogens or have the tropism switching mechanism that has been described for BPP-1. Bacteriophage RW also exhibits some homology to BPP-1. However, it is quite different from the other three phages, and we propose that it should be considered a representative of a third species of the genus Rauchvirus. Taken together, the differences among these four members of the genus Rauchvirus indicate that this divergent genus has a long evolutionary history and that there are many more rauchviruses waiting to be discovered.
View details for DOI 10.1007/s00705-020-04791-4
View details for Web of Science ID 000565107300001
View details for PubMedID 32870405
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Plant growth enhancement is not a conserved feature in the Caulobacter genus
PLANT AND SOIL
2020; 449 (1-2): 81-95
View details for DOI 10.1007/s11104-020-04472-w
View details for Web of Science ID 000517720400002
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The Isolation and Characterization of Kronos, a Novel Caulobacter Rhizosphere Phage that is Similar to Lambdoid Phages
CURRENT MICROBIOLOGY
2019; 76 (5): 558-565
Abstract
Despite their ubiquity, relatively few bacteriophages have been characterized. Here, we set out to explore Caulobacter bacteriophages (caulophages) in the rhizosphere and characterized Kronos, the first caulophage isolated from the rhizosphere. Kronos is a member of the Siphoviridae family since it has a long flexible tail. In addition, an analysis of the Kronos genome indicated that many of the predicted proteins were distantly related to those of bacteriophages in the lambdoid family. Consistent with this observation, we were able to demonstrate the presence of cos sites that are similar to those found at the ends of lambdoid phage genomes. Moreover, Kronos displayed a relatively rare head and tail morphology compared to other caulophages but was similar to that of the lambdoid phages. Taken together, these data indicate that Kronos is distantly related to lambdoid phages and may represent a new Siphoviridae genus.
View details for DOI 10.1007/s00284-019-01656-1
View details for Web of Science ID 000464849800005
View details for PubMedID 30810780
View details for PubMedCentralID PMC6459719
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Achieving Accurate Sequence and Annotation Data for Caulobacter vibrioides CB13
CURRENT MICROBIOLOGY
2018; 75 (12): 1642-1648
Abstract
Annotated sequence data are instrumental in nearly all realms of biology. However, the advent of next-generation sequencing has rapidly facilitated an imbalance between accurate sequence data and accurate annotation data. To increase the annotation accuracy of the Caulobacter vibrioides CB13b1a (CB13) genome, we compared the PGAP and RAST annotations of the CB13 genome. A total of 64 unique genes were identified in the PGAP annotation that were either completely or partially absent in the RAST annotation, and a total of 16 genes were identified in the RAST annotation that were not included in the PGAP annotation. Moreover, PGAP identified 73 frameshifted genes and 22 genes with an internal stop. In contrast, RAST annotated the larger segment of these frameshifted genes without indicating a change in reading frame may have occurred. The RAST annotation did not include any genes with internal stop codons, since it chose start codons that were after the internal stop. To confirm the discrepancies between the two annotations and verify the accuracy of the CB13 genome sequence data, we re-sequenced and re-annotated the entire genome and obtained an identical sequence, except in a small number of homopolymer regions. A genome sequence comparison between the two versions allowed us to determine the correct number of bases in each homopolymer region, which eliminated frameshifts for 31 genes annotated as frameshifted genes and removed 24 pseudogenes from the PGAP annotation. Both annotation systems correctly identified genes that were missed by the other system. In addition, PGAP identified conserved gene fragments that represented the beginning of genes, but it employed no corrective method to adjust the reading frame of frameshifted genes or the start sites of genes harboring an internal stop codon. In doing so, the PGAP annotation identified a large number of pseudogenes, which may reflect evolutionary history but likely do not produce gene products. These results demonstrate that re-sequencing and annotation comparisons can be used to increase the accuracy of genomic data and the corresponding gene annotation.
View details for DOI 10.1007/s00284-018-1572-3
View details for Web of Science ID 000447654300013
View details for PubMedID 30259084
View details for PubMedCentralID PMC6232633