Source: UNIV OF HAWAII submitted to NRP
RAPID ASSESSMENT OF SOIL BIODIVERSITY ACROSS DIVERSE SOIL TYPES AND MANAGEMENT SYSTEMS
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
COMPLETE
Funding Source
Reporting Frequency
Annual
Accession No.
1022247
Grant No.
2020-67020-31173
Cumulative Award Amt.
$196,628.00
Proposal No.
2019-06530
Multistate No.
(N/A)
Project Start Date
Jun 1, 2020
Project End Date
May 31, 2023
Grant Year
2020
Program Code
[A1401]- Foundational Program: Soil Health
Recipient Organization
UNIV OF HAWAII
3190 MAILE WAY
HONOLULU,HI 96822
Performing Department
Tropical Plant & Soil Sciences
Non Technical Summary
Measuring total soil biodiversity is one of the most basic, yet fundamental concepts that can contribute towards an integrative measure of soil health. However, currently there is no system that could quickly and effectively identify the immense biodiversity in soil. Leveraging available high-throughput sequencing technology and bioinformatic tools, this Seed proposal will 1) develop and test a series of ribosomal marker genes that can be sequenced together to identify major groups of soil organisms including bacteria, archaea, fungi, arbuscular mycorrhizal fungi, unicellular eukaryotes (protists), oomycetes, nematodes, and invertebrates; and 2) develop and streamline a flexible and transferable molecular identification system that will enable rapid identification of total soil biodiversity. These tools will be benchmarked using a set of 66 soil samples that came from different soil types, management systems, and disturbance frequencies. The resulting biodiversity measurements (richness, phylogenetic, and functional) will provide the first comprehensive examples of how biodiversity measures can provide insights into what makes a healthy soil, and provide supporting data for developing work in the field of Soil Health.
Animal Health Component
30%
Research Effort Categories
Basic
30%
Applied
30%
Developmental
40%
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
10101101060100%
Knowledge Area
101 - Appraisal of Soil Resources;

Subject Of Investigation
0110 - Soil;

Field Of Science
1060 - Biology (whole systems);
Goals / Objectives
The main goal of this project is to develop a molecular identification system that could quickly and efficiently identify all living organisms in any given soil. Successful development will allow rapid identification of total biodiversity in any soil systems that could immediately support incorporation of soil biodiversity into the various developing concepts in soil health. This project will start with two objectives:Objective 1: Develop a multiplex PCR system that is able to sequence ribosomal RNA genes from major groups of soil organisms (bacteria, archaea, fungi, arbuscular mycorrhizae, unicellular eukaryotes (protists), oomycetes, nematodes, and invertebrates) in a single sequencing run. This includes development and optimization of various protocols to sequence each group of organism individually and together as a single unit.Objective 2: Develop bioinformatic tools and workflows to handle large and diverse datasets, and streamline the tools to enable rapid identification of total soil biodiversity.
Project Methods
Soil collection: From a project aimed at understanding the components of soil health and develop a soil health metric, a total of 22 field sites were sampled in Hawaii, with three replications at each field site for a total of 66 soil samples. These sites span a broad range of six soil Orders (Andisols, Inceptisols, Mollisols, Oxisols, Ultisols, and Vertisols), management practices (conventional and organic), and disturbance history (pasture land, cultivated land, and native forest). Each of these dimensions are replicated at least three times. Collaborations with local farmers provided a rich environment to study soil health across a diverse soil backgrounds and management practices.Molecular markers gene of interests: A series of carefully-selected ribosomal markers based on literature review for their ability to best capture overall diversity in their respective groups will be used to sequence major groups of soil organisms (Table 1). Viruses are excluded because there are no conserved markers and are beyond the scope of this proposal. Preliminary data from our lab identifying nematodes from compost samples showed that the commonly used 18S primer pair (NF1 and 18Sr2b) was able to amplify 8 species of nematodes and the ITS primer pair (M2646-SHITS2R) was able to amplify 5 species, with only 1 species overlapping across these primers. Therefore, we will use three primer pairs to maximize detection of the diversity of nematodes following the recommendation of Porazinska et al., (2009).Organism grouprRNA genePrimersReferenceBacteria & Archaea16S515F-806R(Parada et al., 2016);(Apprill et al., 2015)FungiITSITS1F-ITS2(Gardes and Bruns, 1993);(White et al., 1990)Arbuscular Mycorrhizae18SWANDA-AML2?(Lee et al., 2008); (Dumbrell et al., 2011)Protists18S1389F-EukBr(Amaral-Zettler et al., 2009; Stoeck et al., 2010)OomycetesITSITS3oo-ITS4ngs(Riit et al., 2016)Metazoa18SSSU_FO4-SSU_R22(Fonseca et al., 2010)Nematodes18S28SITSNF1 and 18Sr2bD3A-D3BM2646F-SHITS2R(Mullin et al., 2003; Porazinska et al., 2009)(Nunn, 1992; Porazinska et al., 2009)Table 1: A series of primers that will be used in this proposed project.Table 1: A series of primers that will be used in this proposed project.Molecular identification of soil biodiversity: DNA will be extracted from these 66 soil samples using an established DNA extraction method that PI Nguyen developed that works well for a broad range of soil, including Oxisols and Andisols that have high DNA binding affinity. The Nguyen Lab's standard amplicon sequencing protocol will be used to amplify, barcode, and sequence each gene across all soil samples (Nguyen, 2019a). Amplified and barcoded product from each primer pair will be combined in equimolar concentration to form a single "gene library." There will be a total of nine gene libraries. These libraries will be combined at equimolar concentration into a single master library, which will then be sequenced using 300 bp paired-ends Illumina MiSeq. As a proof of concept, this protocol has been tested multiple times and have worked consistently well for three ribosomal genes (16S - prokaryotes, 18S - protists, ITS - fungi) and yielded an average of 31,000 sequences per sample, in MiSeq run with 250 samples.Multiplex PCR to assess total biodiversity: In order to streamline identification of soil organisms across many samples, we will use multiplex PCR where multiple primers will be combined into a single cocktail and used in a single PCR reaction. This method has been successfully used successfully in various systems (Oliveira and de Lencastre, 2002;Felske et al., 2003; Solà et al., 2018) and preliminary data in our lab showed that at least three primers could be multiplexed. However, a complex mixture of nine primers will need to be benchmarked using the 66 soil samples. We will use the same PCR amplification strategy as above, with the only difference being primer annealing temperature 64-52 °C (touch-down PCR) to mitigate primer binding and competition biases. We will also optimize of other parameters known to affect multiplex PCR (Edwards and Gibbs, 1994; Henegariu et al., 1997). Each of the 66 samples will then be barcoded to identify them and sequenced using Illumina MiSeq as above.AnalysesSequences will undergo a series of rigorous bioinformatics quality control steps using QIIME2 (Bolyen et al., 2019). Detailed pipeline in general for 16S, 18S, and ITS ribosomal markers has been refined by PI Nguyen and is adaptable to any primer sets (Nguyen, 2019b). To assess overall biodiversity, we will measure operational taxonomic units (OTUs), Faith's Phylogentic Diversity for conserved 16S and 18S genes (ITS is too variable to for this metric), Chao2 estimated richness, and Shannon's Index. These diversity metrices will be statistically compared among the soil types, management, disturbance regimes, and other environmental variables available in our soil dataset. Community description will be visualized using PCoA and/or NMDS and statistically compared using PERMANOVA based analyses.Functional diversity using trophic guild (who eats whom) will be measured and compared as above for fungi (Nguyen et al. 2016), protists (Xiong et al., 2018), nematodes (Sieriebriennikov et al., 2014), mites (Birkhofer et al., 2016, de Groot et al., 2016) and general soil fauna (Ehnes et al., 2011). To identify taxa that occur in one environment but not another (in other words, indicator taxa) that might provide insights into soil health, we will employ a robust method called Analysis of Composition of Microbiomes (ANCOM) that uses compositional constraints to reduce false discoveries (Mandal et al., 2015).A framework using co-occurrence network analysis will be used to connect OTUs from all these different experimental soil data together (Williams et al., 2014; Freilich et al., 2018). Cross-amplicon (functionally cross-kingdom) networks, although are at an infancy and still require further development, can serve as a powerful way to connect the richness of organisms in the soil environment. We have developed a method based on (Tipton et al., 2018) to produce fungal-bacterial networks that hypothesize relationships among the different taxa in a dataset (Fig 3). Network analyses can integrate nearly infinite data including taxonomic and functional data to explore co-occurrence and potential interactions, while network structure, such as network complexity, might inform about the state of a system (e.g. how healthy a soil might be). For instance, natural and stable systems have been associated with a more complex soil biodiversity network compared to agricultural and less stable systems (Morriën et al., 2017; de Araujo et al., 2018; Banerjee et al., 2019), and our work showed that organic fertilizers creates a more stable network than mineral fertilizers.Sequence data from the multiplexed PCR experiment will be processed as above. Richness, Phylogenetic Diversity, Chao2 richness estimator, Shannon's Diversity index, community similarity, functional diversity, and network integrity will be correlated to the previous dataset. Correlations among these datasets (from Objective 1~Objective 2) will allow us to measure the robustness of this multiplex PCR dataset, and provide insights into whether results from multiplexed PCRs have enough integrity to measure total soil biodiversity.

Progress 06/01/20 to 05/31/23

Outputs
Target Audience:The target audience for this project is primarily the research community. A portion of the findings from this project has been communicated to this audience. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?Training activities This research provided training for: 3 postdoctoral researchers (1.7 FTE) 2 graduate students (0.7 FTE) 5 undergraduate students (2 FTE) Professional development This grant provided opportunities for the PI, a postdoc, and 2 graduate students to attend various professional development activities: National conferences: Ecological Society of America, Mycological Society of America, Soil Ecology Society Workshops and seminars: The CalTech Rhizosphere Workshop, Global Soil Biodiversity Initiative monthly seminar, KBase workshop on taxonomic profiling using genomes, Harvard Fungal Symposium, Global Soil Biodiversity Initiative monthly seminar, EMSL Summer School for bioinformatic analysis, Antimicrobial Resistance bioinformatic workshop. How have the results been disseminated to communities of interest?The results have been disseminated through both written and oral means: 1 published peer-reviewed paper, led by a graduate student (Heisey) 3 invited conference oral paper, 1 delivered by graduate student (Dhungana), 2 delivered by PI (Nguyen). One of the seminars delivered by PI Nguyen was to a Canadian group managing a large research portfolio on the human microbiome and human health; the other was to the National Academies on their study on the connection between Soil Health and Human Health. 1 contributed oral presentations at a national scientific conference, delivered by a graduate student (Dhungana) 2 posters at a university-led event, delivered by undergraduate students (Lee, Rich) 1 public radio presentation by PI (Nguyen) What do you plan to do during the next reporting period to accomplish the goals? Nothing Reported

Impacts
What was accomplished under these goals? Overall Impact We found that primer multiplexing to identify soil biodiversity is a viable technique. With further optimization, it could be developed into a system that provides a quick and low-cost alternative to identify the tremendous biodiversity in soils. In application, it may be integrated into any existing system (such as those in soil testing centers) to measure and monitor soil health across the country. As there is increasing interest from stake-holders in soil biolog's connection to crop systems, further development of this method will help us respond to this need, as well as supporting the science connecting soil microorganisms to soil health and plant productivity. Objective 1: Develop a multiplex PCR system 1) Major activities completed / experiments conducted We developed two additional nematode primer sets (18S and ITS regions of the rRNA gene) to compliment available primers in the literature. These additional primer sets provided more flexibility to identify nematode diversity in soil. We tested and attempted to optimize a multiplex PCR method. We mixed 6 primer sets in various combinations from individual primer to a complex set of all 6 primers. We found various efficiencies associated with these mixes and note that further optimization is needed. We applied our method to amplify and identify the biota in 24 soil samples collected from 4 agricultural management systems (native forest, unmanaged lands, conventional management, organic management). We found that XXX 2) Data collected We collected three sets of DNA sequence data: 1) nematode DNA sequences that we developed (145,605 sequences), 2) multiplex primer system test (14,700,761 sequences), and 3) soils across management practices (36,948,258) sequences. These data were processed using the developed bioinformatics pipeline (see Objective 2 below). 3) Summary statistics and discussion of results Strengths: We found that the primer multiplex method performs just as well as the traditional, individual primer method to detect dominant taxa in the soil. This is true for alpha-diversity (supported by the stability of the Simpson Diversity Index), and to our surprise for beta-diversity (supported by PERMANOVA analyses). Limitations: The multiplex primer method tends to underestimate the alpha diversity for most taxa, especially the rare ones. This may be due to reduced sequencing power when primers are combined. If this is true, increase sequencing power (more sequences per sample) should solve this issue. In addition, we found that primers for oomycetes did not work well. Since the development of this project, new primers are available in the literature that can help solve this issue. Future developments: Primer optimization could lead to better performance and predictability. 4) Key outcomes or other accomplishments realized We are excited to report that we have successfully developed a viable system for detecting total soil biodiversity. Currently the system works, but with some optimization, it could be deployed broadly. We are optimistic for the continued development and broader deployment of this system. Objective 2: Develop bioinformatic tools and workflows 1) Major activities completed / experiments conducted We adapted a previous pipeline, and from there, restructure the pipeline such that it can effectively handle the many types of organisms in this study. This required building new databases, testing, and optimization of work flow. 2) Data collected The pipeline generated data in various formats. Many of these are standard bioinformatic formats, stored as text files. These files can be reproduced by any computer using the same software and workflow. 3) Summary statistics and discussion of results Strengths: The pipeline allowed us to reproducibly identify the major groups of soil organisms in soils from Objective 1. It operates with moderate efficiency. Limitations: A portion of the pipeline is not automated, and thus a human is still required to run the pipeline. Future developments: Optimization and automation of the pipeline and integration into a website that could be made available to anyone with internet access. 4) Key outcomes or other accomplishments realized We have successfully developed a bioinformatic pipeline that is able to handle multiplex primer sets. Currently, the analysis pipeline provides an easily adaptable, reproducible, and reliable means of assessing community structure of prokaryotes, fungi, nematodes, and protists.

Publications

  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2022 Citation: Rich, K., Dhungana, I., and Nguyen, N. (2022) Soil Nutrients Vary with Soil Depth in Tropical Oxisols. Summer Undergraduate Research Experience (SURE) Symposium, University of Hawaii at Manoa.
  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2022 Citation: Lee, S. and Nguyen, N. (2022) Development and Applying High-throughput Bacterial Isolation from Environmental Samples to Study Oxalotrophic Bacteria Associated with Fungal Mats. Summer Undergraduate Research Experience (SURE) Symposium, University of Hawaii at Manoa.
  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2023 Citation: Nguyen, N.H. (2023) The Soil Microbiome: Connecting Soil Health to Human Health. (2023). Canadian Institute for Advanced Research (CIFAR) Human & the Microbiome (HMB) meeting. Banff, Canada.
  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2023 Citation: Nguyen, N.H. (2023) Connecting the Soil Microbiome to Human Health. The National Academies for Science, Engineering, and Medicine study Exploring Linkages Between Soil Health and Human Health. Washington DC.


Progress 06/01/21 to 05/31/22

Outputs
Target Audience:A portion of the findings from this project has been communicated to members of the scientific community. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?Training activities This project provided training for 1 postdoctoral researcher, 1 graduate student, and 1 undergraduate students. Professional development This grant provided opportunities for the PI and a graduate students to attend various professional development activities: National conferences: Soil Ecology Society conference Workshops and seminars: Global Soil Biodiversity Initative montly seminar, EMSL Summer School for bioinformatic analysis How have the results been disseminated to communities of interest?One paper was published in the open-access journal Frontiers in Soil Science, led by a graduate student. One oral presentation was given at the Soil Ecology Society meeting, given by a graduate student. What do you plan to do during the next reporting period to accomplish the goals?We plan to wrap up this project with the following tasks: Complete data analysis Write and publish a manuscript that highlights the main findings of this project Present the results at a conference (potentially the 3rd Global Soil Biodiversity Conference in Dublin, Ireland in 2023)

Impacts
What was accomplished under these goals? Overall Impact: In this project, we showed that primer multiplexing to identify soil biodiversity is a viable technique. With further optimization, it could be developed into a system that provides a quick and low-cost alternative to identify the biodiversity in soils. In application, it may be integrated into any existing system (such as those in soil testing centers) to measure and monitor soil health across the country. Objective 1: This objective has been completed. In the previous report, we summarized our method and findings. In brief, we found that our multiplex PCR system is a viable option to quickly detect and identify soil biota, including but not limated to soil bacteria, fungi, and nematodes. We used our developed method to sequence the soil biota in 24 samples of soils collected from 4 agricultural management systems. We have sequenced the DNA from these soils and the dataset is being analyzed. Objective 2: This objective has been completed. In the previous report, we summarized our method and findings. In brief, we have produced and stream-lined a bioinformatic pipeline that is able to handle large and complex datasets. We are applying this pipeline to analyze the last component of the project from Objective 1.

Publications

  • Type: Journal Articles Status: Published Year Published: 2022 Citation: Heisey S, Ryals R, Maaz TM and Nguyen NH (2022) A Single Application of Compost Can Leave Lasting Impacts on Soil Microbial Community Structure and Alter Cross-Domain Interaction Networks. Front. Soil Sci. 2:749212. doi: 10.3389/fsoil.2022.749212
  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2022 Citation: Dhungana I and Nguyen NH (2021) Do plant species and their root exudates influence soil microbes in a tropical soil? Oral presentation at the Soil Ecology Society meeting in Richland, WA.


Progress 06/01/20 to 05/31/21

Outputs
Target Audience:A portion of the findings from this project has been communicated to members of the scientific community. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?Training activities This research provided training for 1 postdoctoral researcher, 1 graduate student, and 2 undergraduate students. Professional development This grant provided opportunities for the PI, a postdoc, and 2 graduate students to attend various professional development activities: National conferences: Ecological Society of America, Mycological Society of America Workshops and seminars: The CalTech Rhizosphere Workshop, Global Soil Biodiversity Initative montly seminar, KBase workshop on taxonomic profiling using genomes, Harvard Fungal Symposium How have the results been disseminated to communities of interest?One paper was submitted and in review, led by a graduate student. One invited conference seminar was given by a graduate student. What do you plan to do during the next reporting period to accomplish the goals?We plan to: Optimize primer multiplexing system so that we could produce stable and reliable results. Apply this system to study soil biodiversity across different management systems. Publish a manuscript describing the method and application. Present result at conference(s).

Impacts
What was accomplished under these goals? Impact As this is the first year of the project, there is no impact to report yet. Objective 1: 1) Major activities completed / experiments conducted We developed two additional nematode primer sets (18S and ITS regions of the rRNA gene) to compliment what has already been developed in the literature. This is important to be able to describe nematode diversity in soils due to the high diversity of this group of organisms. We have begun developing a multiplex PCR system. We mixed 6 primer sets in various combinations from individual primers to a complex set of all 6 primers. These primer sets were used to amplify a compost sample that had been spiked with various groups of organisms including oomycetes and plant parasitic nematodes. This is to ensure that all major groups of soil organisms were represented. We successfully amplified all samples and sequenced them using high-throughput Illumina sequencing. 2) Data collected We collected two sets of DNA sequence data: 1) nematode primers that we developed (145,605 sequences) and 2) multiplex primer system (14,700,761 sequences) 3) Summary statistics and discussion of results The new nematode primers performed as expected and captured a good proportion of diversity. However, different primer sets will capture different groups of nematodes with little overlap. Therefore, we concluded that multiple primer sets are necessary in order to capture total nematode diversity. We used these primers in the multiplex primer system. The multiplex primers worked well in general, but with some inconsistencies were found. Fungal diversity was relatively thoroughly captured when the fungal ITS primers were multiplexed with primers for various other target genes. Protist diversity was also relatively thoroughly captured when protist primers were multiplexed with primers for fungal ITS and/or prokaryotes and oomycetes. However, incorporation of nematode 18S or ITS primers significantly impacted protist richness. The current analysis of preliminary data suggests that prokaryotic and nematode community diversity estimates were heavily influenced by multiplexing. The next step in this process is to tweak parameters and primer mixes to balance out diversity estimates. Once that is done, we will apply the balanced primer mix to a set of soils across agricultural management systems. 4) Key outcomes or other accomplishments realized To fully capture nematode diversity, we recommend that multiple primer sets be used. The complex primer sets appears to be working, and with further development could provide a low-cost system for identification of all major groups of soil microorganisms. Objective 2: 1) Major activities completed / experiments conducted We developed a bioinformatic pipeline that is able to handle multiple primer sets. Currently, the analysis pipeline provides an easily adaptable, reproducible, and reliable means of assessing community structure and diversity of prokaryotes, fungi, nematodes, and protists. The whole pipeline will be made publically available with the first publication that results from this project. 2) Data collected The pipeline allowed us to identify the major groups of soil orgamisms in our test sample from Objective 1. We were able to measure species richness, and the efficacy of this primer-multiplexing approach. 3) Summary statistics and discussion of results Fungal was relatively thoroughly captured when the fungal ITS primers were multiplexed with primers for various other target genes. Protist diversity was also relatively thoroughly captured when protist primers were multiplexed with primers for fungal ITS and/or prokaryotes and oomycetes. However, incorporation of nematode 18S or ITS primers significantly impacted protist richness estimates. The current analysis of preliminary data suggests that prokaryotic and nematode community diversity estimates were heavily influenced by multiplexing. 4) Key outcomes or other accomplishments realized Primer multiplexing to identify total soil biodiversity works -- we are happy to report that this approach appears to be very viable and with further optimization, could be employed as a quick and low-cost alternative to identify total soil biodiversity in any soil sample.

Publications

  • Type: Journal Articles Status: Submitted Year Published: 2021 Citation: Heisey, S., Ryals, R., McClellan Maaz, T., and Nguyen, N.H. 2021. Complex, high-nitrogen fertilizers can leave lasting impacts and alter cross-domain interaction networks. Submitted to Applied and Environmental Microbiology.
  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2021 Citation: Dhungana, I. and Nguyen, N.H. 2021. Soil microbial community coalescence in continuous cropping. Ecological Society of America, 2021 Annual Meeting, online.