Publications

@article{Diamond2019,

title = {Mediterranean grassland soil C–N compound turnover is dependent on rainfall and depth, and is mediated by genomically divergent microorganisms.},

author = {Spencer Diamond and Peter F. Andeer and Zhou Li and Alexander Crits-Christoph and David Burstein and Karthik Anantharaman and Katherine R. Lane and Brian C. Thomas and Chongle Pan and Trent R. Northen and Jillian F. Banfield},

url = {https://angelo.berkeley.edu/wp-content/uploads/sites/59/41564_2019_Article_449.pdf},

doi = {10.1038/s41564-019-0449-y},

year  = {2019},

date = {2019-05-20},

journal = {Nature Microbiology},

volume = {4},

pages = {1356-1367},

abstract = {Soil microbial activity drives the carbon and nitrogen cycles and is an important determinant of atmospheric trace gas turnover, yet most soils are dominated by microorganisms with unknown metabolic capacities. Even Acidobacteria, among the most abundant bacteria in soil, remain poorly characterized, and functions across groups such as Verrucomicrobia, Gemmatimonadetes, Chloroflexi and Rokubacteria are understudied. Here, we have resolved 60 metagenomic and 20 proteomic data sets from a Mediterranean grassland soil ecosystem and recovered 793 near-complete microbial genomes from 18 phyla, representing around one-third of all microorganisms detected. Importantly, this enabled extensive genomics-based metabolic predictions for these communities. Acidobacteria from multiple previously unstudied classes have genomes that encode large enzyme complements for complex carbohydrate degradation. Alternatively, most microorganisms encode carbohydrate esterases that strip readily accessible methyl and acetyl groups from polymers like pectin and xylan, forming methanol and acetate, the availability of which could explain the high prevalence of C1 metabolism and acetate utilization in genomes. Microorganism abundances among samples collected at three soil depths and under natural and amended rainfall regimes indicate statistically higher associations of inorganic nitrogen metabolism and carbon degradation in deep and shallow soils, respectively. This partitioning decreased in samples under extended spring rainfall, indicating that long-term climate alteration can affect both carbon and nitrogen cycling. Overall, by leveraging natural and experimental gradients with genome-resolved metabolic profiles, we link microorganisms lacking prior genomic characterization to specific roles in complex carbon, C1, nitrate and ammonia transformations, and constrain factors that impact their distributions in soil.},

keywords = {ERCZO, metagenomics, soil microbes},

pubstate = {published},

tppubtype = {article}

}

@article{Crits-Christoph2018,

title = {Novel soil bacteria possess diverse genes for secondary metabolite biosynthesis},

author = {Alexander Crits-Christoph and Spencer Diamond and Cristina N. Butterfield and Brian C. Thomas and Jillian F. Banfield},

doi = {10.1038/s41586-018-0207-y},

year  = {2018},

date = {2018-06-13},

journal = {Nature},

volume = {558},

pages = {440-444},

abstract = {In soil ecosystems, microorganisms produce diverse secondary metabolites such as antibiotics, antifungals and siderophores that mediate communication, competition and interactions with other organisms and the environment. Most known antibiotics are derived from a few culturable microbial taxa, and the biosynthetic potential of the vast majority of bacteria in soil has rarely been investigated. Here we reconstruct hundreds of near-complete genomes from grassland soil metagenomes and identify microorganisms from previously understudied phyla that encode diverse polyketide and nonribosomal peptide biosynthetic gene clusters that are divergent from well-studied clusters. These biosynthetic loci are encoded by newly identified members of the Acidobacteria, Verrucomicobia and Gemmatimonadetes, and the candidate phylum Rokubacteria. Bacteria from these groups are highly abundant in soils, but have not previously been genomically linked to secondary metabolite production with confidence. In particular, large numbers of biosynthetic genes were characterized in newly identified members of the Acidobacteria, which is the most abundant bacterial phylum across soil biomes5. We identify two acidobacterial genomes from divergent lineages, each of which encodes an unusually large repertoire of biosynthetic genes with up to fifteen large polyketide and nonribosomal peptide biosynthetic loci per genome. To track gene expression of genes encoding polyketide synthases and nonribosomal peptide synthetases in the soil ecosystem that we studied, we sampled 120 time points in a microcosm manipulation experiment and, using metatranscriptomics, found that gene clusters were differentially co-expressed in response to environmental perturbations. Transcriptional co-expression networks for specific organisms associated biosynthetic genes with two-component systems, transcriptional activation, putative antimicrobial resistance and iron regulation, linking metabolite biosynthesis to processes of environmental sensing and ecological competition. We conclude that the biosynthetic potential of abundant and phylogenetically diverse soil microorganisms has previously been underestimated. These organisms may represent a source of natural products that can address needs for new antibiotics and other pharmaceutical compounds.},

keywords = {ERCZO, metagenomic sequencing, soil microbes},

pubstate = {published},

tppubtype = {article}

}

@article{Butterfield2016,

title = {Proteogenomic analyses indicate bacterial methylotrophy and archaeal heterotrophy are prevalent below the grass root zone.},

author = {Cristina N. Butterfield and Zhou Li and Peter F. Andeer and Susan Spaulding and Brian C. Thomas and Andrea Singh and Robert L. Hettich and Kenwyn B. Suttle and Alexander J. Probst and Susannah G. Tringe and Trent Northen and Chongle Pan and Jillian F. Banfield},

url = {https://angelo.berkeley.edu/peerj-2687-2/},

doi = {10.7717/peerj.2687},

year  = {2016},

date = {2016-11-08},

journal = {PeerJ},

volume = {4},

pages = {e2687},

abstract = {Annually, half of all plant-derived carbon is added to soil where it is microbially respired to 

CO2. However, understanding of the microbiology of this process is limited because most 

culture-independent methods cannot link metabolic processes to the organisms present, 

and this link to causative agents is necessary to predict the results of perturbations on the 

system. We collected soil samples at two sub-root depths (10 – 20 cm and 30 – 40 cm) 

before and after a rainfall-driven nutrient perturbation event in a Northern California 

grassland that experiences a Mediterranean climate. From ten samples, we reconstructed 

198 metagenome-assembled genomes that represent all major phylotypes. We also 

quantified 6,835 proteins and 175 metabolites and showed that after the rain event the 

concentrations of many sugars and amino acids approach zero at the base of the soil 

profile. Unexpectedly, the genomes of novel members of the Gemmatimonadetes and 

Candidate Phylum Rokubacteria phyla encode pathways for methylotrophy. We infer that 

these abundant organisms contribute substantially to carbon turnover in the soil, given 

that methylotrophy proteins were among the most abundant proteins in the proteome. 

Previously undescribed Bathyarchaeota and Thermoplasmatales archaea are abundant in 

deeper soil horizons and are inferred to contribute appreciably to aromatic amino acid 

degradation. Many of the other bacteria appear to breakdown other components of plant 

biomass, as evidenced by the prevalence of various sugar and amino acid transporters and 

corresponding hydrolyzing machinery in the proteome. Overall, our work provides 

organism-resolved insight into the spatial distribution of bacteria and archaea whose 

activities combine to degrade plant-derived organics, limiting the transport of methanol, 

amino acids and sugars into underlying weathered rock. The new insights into the soil carbon cycle during an intense period of carbon turnover, including biogeochemical roles to previously little known soil microbes, were made possible via the combination of metagenomics, proteomics, and metabolomics.},

keywords = {ERCZO, metagenomics, northern California, soil microbes},

pubstate = {published},

tppubtype = {article}

}

@article{Cruz-Martinez2012,

title = {Effect of rainfall-induced soil geochemistry dynamics on grassland soil microbial communities},

author = {K Cruz-Martinez and A Rosling and Y Zhang and M Song and GL Andersen and JF Banfield},

url = {http://aem.asm.org/content/early/2012/08/13/AEM.00203-12},

doi = {10.1128/AEM.00203-12},

issn = {0099-2240, 1098-5336},

year  = {2012},

date = {2012-08-17},

journal = {Applied and Environmental Microbiology},

abstract = {In Mediterranean-type grassland ecosystems, the timing of rainfall events control biogeochemical cycles as well as phenology and productivity of plants and animals. Here, we investigate the effect of short-term (days) soil environmental condition on microbial community structure and composition during a natural wetting and drying cycle. Soil samples were collected from a meadow in Northern California at four time points after the first two rainfall events of the rainy season. We used the 16S rRNA microarrays (PhyloChip) to track changes in bacterial and archaeal community composition. Microbial communities at time points one and three were significantly different than communities at time points two and four. Based on ordination analysis, available carbon, soil moisture and temperature explained most of the variation in community structure. For the first time, a complementary and more comprehensive approach using linear regression (LR) and generalized logical networks (GLN) were used to identify linear and non-linear associations among environmental variables and with the relative abundance of sub-families. Changes in soil moisture and available carbon were correlated with the relative abundance of many Phyla. Only the phylum Actinobacteria showed a lineage specific relationship to soil moisture but not to carbon or nitrogen. The results indicate that use of high taxonomic rank in correlations with nutritional indicators might obscure divergent sub-family-level responses to environmental parameters. An important implication of this research is that there is short-term variation in microbial community composition driven in part by rainfall fluctuation that may not be evident in long-term studies with coarser time resolution.},

keywords = {soil microbes},

pubstate = {published},

tppubtype = {article}

}