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Genome-Resolved Metagenomics Reveals Distinct Phosphorus Acquisition Strategies between Soil Microbiomes.

ABSTRACT: Enhancing soil phosphate solubilization is a promising strategy for agricultural sustainability, while little is known about the mechanisms of how microorganisms cope with differing phosphorus availability. Using a combination of genome-resolved metagenomics and amplicon sequencing, we investigated the microbial mechanisms involved in phosphorus cycling under three agricultural treatments in a wheat-maize rotation system and two natural reforestation treatments. Available soil phosphorus was the key factor shaping bacterial and fungal community composition and function across our agricultural and reforestation sites. Membrane-bound quinoprotein glucose dehydrogenase (PQQGDH) and exopolyphosphatases (PPX) governed microbial phosphate solubilization in agroecosystems. In contrast, genes encoding glycerol-3-phosphate transporters (ugpB, ugpC, and ugpQ) displayed a significantly greater abundance in the reforestation soils. The gcd gene encoding PQQGDH was found to be the best determinant for bioavailable soil phosphorus. Metagenome-assembled genomes (MAGs) affiliated with Cyclobacteriaceae and Vicinamibacterales were obtained from agricultural soils. Their MAGs harbored not only gcd but also the pit gene encoding low-affinity phosphate transporters. MAGs obtained from reforestation soils were affiliated with Microtrichales and Burkholderiales. These contain ugp genes but no gcd, and thereby are indicative of a phosphate transporter strategy. Our study demonstrates that knowledge of distinct microbial phosphorus acquisition strategies between agricultural and reforestation soils could help in linking microbial processes with phosphorus cycling. IMPORTANCE The soil microbiome is the key player regulating phosphorus cycling processes. Identifying phosphate-solubilizing bacteria and utilizing them for release of recalcitrant phosphate that is bound to rocks or minerals have implications for improving crop nutrient acquisition and crop productivity. In this study, we combined functional metagenomics and amplicon sequencing to analyze microbial phosphorus cycling processes in natural reforestation and agricultural soils. We found that the phosphorus acquisition strategies significantly differed between these two ecosystems. A microbial phosphorus solubilization strategy dominated in the agricultural soils, while a microbial phosphate transporter strategy was observed in the reforestation soils. We further identified microbial taxa that contributed to enhanced phosphate solubilization in the agroecosystem. These microbes are predicted to be beneficial for the increase in phosphate bioavailability through agricultural practices.

SUBMITTER: Wu X

PROVIDER: S-EPMC8751388 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:The functioning, health, and productivity of soil are intimately tied to a complex network of interactions, particularly in plant root-associated rhizosphere soil. We conducted a stable-isotope-informed, genome-resolved metagenomic study to trace carbon from Avena fatua grown in a 13CO2 atmosphere into soil. We collected paired rhizosphere and nonrhizosphere soil at 6 and 9 weeks of plant growth and extracted DNA that was then separated by density using ultracentrifugation. Thirty-two fractions from each of five samples were grouped by density, sequenced, assembled, and binned to generate 55 unique bacterial genomes that were ≥70% complete. We also identified complete 18S rRNA sequences of several 13C-enriched microeukaryotic bacterivores and fungi. We generated 10 circularized bacteriophage (phage) genomes, some of which were the most labeled entities in the rhizosphere, suggesting that phage may be important agents of turnover of plant-derived C in soil. CRISPR locus targeting connected one of these phage to a Burkholderiales host predicted to be a plant pathogen. Another highly labeled phage is predicted to replicate in a Catenulispora sp., a possible plant growth-promoting bacterium. We searched the genome bins for traits known to be used in interactions involving bacteria, microeukaryotes, and plant roots and found DNA from heavily 13C-labeled bacterial genes thought to be involved in modulating plant signaling hormones, plant pathogenicity, and defense against microeukaryote grazing. Stable-isotope-informed, genome-resolved metagenomics indicated that phage can be important agents of turnover of plant-derived carbon in soil. IMPORTANCE Plants grow in intimate association with soil microbial communities; these microbes can facilitate the availability of essential resources to plants. Thus, plant productivity commonly depends on interactions with rhizosphere bacteria, viruses, and eukaryotes. Our work is significant because we identified the organisms that took up plant-derived organic C in rhizosphere soil and determined that many of the active bacteria are plant pathogens or can impact plant growth via hormone modulation. Further, by showing that bacteriophage accumulate CO2-derived carbon, we demonstrated their vital roles in redistribution of plant-derived C into the soil environment through bacterial cell lysis. The use of stable-isotope probing (SIP) to identify consumption (or lack thereof) of root-derived C by key microbial community members within highly complex microbial communities opens the way for assessing manipulations of bacteria and phage with potentially beneficial and detrimental traits, ultimately providing a path to improved plant health and soil carbon storage.

Project description:BackgroundThe production of 1 L of ethanol from sugarcane generates up to 12 L of vinasse, which is a liquid waste containing an as-yet uncharacterized microbial assemblage. Most vinasse is destined for use as a fertilizer on the sugarcane fields because of the high organic and K content; however, increased N2O emissions have been observed when vinasse is co-applied with inorganic N fertilizers. Here we aimed to characterize the microbial assemblage of vinasse to determine the gene potential of vinasse microbes for contributing to negative environmental effects during fertirrigation and/or to the obstruction of bioethanol fermentation.ResultsWe measured chemical characteristics and extracted total DNA from six vinasse batches taken over 1.5 years from a bioethanol and sugar mill in Sao Paulo State. The vinasse microbial assemblage was characterized by low alpha diversity with 5-15 species across the six vinasses. The core genus was Lactobacillus. The top six represented bacterial genera across the samples were Lactobacillus, Megasphaera and Mitsuokella (Phylum Firmicutes, 35-97% of sample reads); Arcobacter and Alcaligenes (Phylum Proteobacteria, 0-40%); Dysgonomonas (Phylum Bacteroidetes, 0-53%); and Bifidobacterium (Phylum Actinobacteria, 0-18%). Potential genes for denitrification but not nitrification were identified in the vinasse metagenomes, with putative nirK and nosZ genes the most represented. Binning resulted in 38 large bins with between 36.0 and 99.3% completeness, and five small mobile element bins. Of the large bins, 53% could be classified at the phylum level as Firmicutes, 15% as Proteobacteria, 13% as unknown phyla, 13% as Bacteroidetes and 6% as Actinobacteria. The large bins spanned a range of potential denitrifiers; moreover, the genetic repertoires of all the large bins included the presence of genes involved in acetate, CO2, ethanol, H2O2, and lactose metabolism; for many of the large bins, genes related to the metabolism of mannitol, xylose, butyric acid, cellulose, sucrose, "3-hydroxy" fatty acids and antibiotic resistance were present based on the annotations. In total, 21 vinasse bacterial draft genomes were submitted to the genome repository.ConclusionsIdentification of the gene repertoires of vinasse bacteria and assemblages supported the idea that organic carbon and nitrogen present in vinasse together with microbiological variation of vinasse might lead to varying patterns of N2O emissions during fertirrigation. Furthermore, we uncovered draft genomes of novel strains of known bioethanol contaminants, as well as draft genomes unknown at the phylum level. This study will aid efforts to improve bioethanol production efficiency and sugarcane agriculture sustainability.

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Project description:Increasing evidence shows that the chicken gastrointestinal microbiota has a major effect on the modulation of metabolic functions and is correlated with economic parameters, such as feed efficiency and health. Some of these effects derive from the capacity of the chicken to digest carbohydrates and produce energy-rich metabolites such as short-chain fatty acids (SCFA) and from host-microbe interactions. In this study, we utilized information from metagenomic assembled genomes (MAGs) from chicken gastrointestinal tract (GIT) samples, with detailed annotation of carbohydrate-active enzymes (CAZymes) and genes involved in SCFA production, to better understand metabolic potential at different ages. Metagenomic sequencing of 751 chicken GIT samples was performed to reconstruct 155 MAGs, representing species which belong to six phyla, primarily Firmicutes followed by Proteobacteria. MAG diversity significantly (p < 0.001) increased with age, with early domination of Lachnospiraceae, followed by other families including Oscillospiraceae. Age-dependent shifts were observed in the abundance of genes involved in CAZyme and SCFA production, exemplified by a significant increase in glycosyltransferases (GTs) and propionic acid production pathways (p < 0.05), and a lower abundance of glycoside hydrolases (GHs) (p < 0.01). Co-occurrence analysis revealed a large cluster highly interconnected by enzymes from GT2_2 and GH3 families, underscoring their importance in the community. Furthermore, several species were identified as interaction hubs, elucidating associations of key microbes and enzymes that more likely drive temporal changes in the chicken gut microbiota, and providing further insights into the structure of the complex microbial community. This study extends prior efforts on the characterization of the chicken GIT microbiome at the taxonomic and functional levels and lays an important foundation toward better understanding the broiler chicken gut microbiome helping in the identification of modulation opportunities to increase animal health and performance.

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Genome-Resolved Metagenomics Reveals Distinct Phosphorus Acquisition Strategies between Soil Microbiomes.

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