Publications

Microbial Populations Are Shaped by Dispersal and Recombination in a Low Biomass Subseafloor Habitat

Published in mBio, 2022

The subseafloor is a vast habitat that supports microorganisms that have a global scale impact on geochemical cycles. Many of the endemic microbial communities inhabiting the subseafloor consist of small populations under growth-limited conditions. For small populations, stochastic evolutionary events can have large impacts on intraspecific population dynamics and allele frequencies. These conditions are fundamentally different from those experienced by most microorganisms in surface environments, and it is unknown how small population sizes and growth-limiting conditions influence evolution and population structure in the subsurface. Using a 2-year, high-resolution environmental time series, we examine the dynamics of microbial populations from cold, oxic crustal fluids collected from the subseafloor site North Pond, located near the mid-Atlantic ridge. Our results reveal rapid shifts in overall abundance, allele frequency, and strain abundance across the time points observed, with evidence for homologous recombination between coexisting lineages. We show that the subseafloor aquifer is a dynamic habitat that hosts microbial metapopulations that disperse frequently through the crustal fluids, enabling gene flow and recombination between microbial populations. The dynamism and stochasticity of microbial population dynamics in North Pond suggest that these forces are important drivers in the evolution of microbial populations in the vast subseafloor habitat.

Recommended citation: Anderson, R. E., Graham, E. D., Huber, J. A. & Tully, B. J. Microbial Populations Are Shaped by Dispersal and Recombination in a Low Biomass Subseafloor Habitat. Mbio e00354-22 (2022) doi:10.1128/mbio.00354-22. https://journals.asm.org/doi/full/10.1128/mbio.00354-22

Potential Phosphorus Uptake Mechanisms in the Deep Sedimentary Biosphere

Published in Frontiers in Marine Science, 2022

Our understanding of phosphorus (P) dynamics in the deep subseafloor environment remains limited. Here we investigate potential microbial P uptake mechanisms in oligotrophic marine sediments beneath the North Atlantic Gyre and their effects on the relative distribution of organic P compounds as a function of burial depth and changing redox conditions. We use metagenomic analyses to determine the presence of microbial functional genes pertaining to P uptake and metabolism, and solution 31P nuclear magnetic resonance spectroscopy (31P NMR) to characterize and quantify P substrates. Phosphorus compounds or compound classes identified with 31P NMR include inorganic P compounds (orthophosphate, pyrophosphate, polyphosphate), phosphonates, orthophosphate monoesters (including inositol hexakisphosphate stereoisomers) and orthophosphate diesters (including DNA and phospholipid degradation products). Some of the genes identified include genes related to phosphate transport, phosphonate and polyphosphate metabolism, as well as phosphite uptake. Our findings suggest that the deep sedimentary biosphere may have adapted to take advantage of a wide array of P substrates and could play a role in the gradual breakdown of inositol and sugar phosphates, as well as reduced P compounds and polyphosphates.

Recommended citation: Defforey D, Tully BJ, Sylvan JB, Cade-Menun BJ, Kiel Reese B, Zinke L and Paytan A (2022) Potential Phosphorus Uptake Mechanisms in the Deep Sedimentary Biosphere. Front. Mar. Sci. 9:907527. doi: 10.3389/fmars.2022.907527 https://www.frontiersin.org/articles/10.3389/fmars.2022.907527/full

The Bioinformatics Virtual Coordination Network: An Open-Source and Interactive Learning Environment

Published in Frontiers in Education, 2021

Lockdowns and “stay-at-home” orders, starting in March 2020, shuttered bench and field dependent research across the world as a consequence of the global COVID-19 pandemic. The pandemic continues to have an impact on research progress and career development, especially for graduate students and early career researchers, as strict social distance limitations stifle ongoing research and impede in-person educational programs. The goal of the Bioinformatics Virtual Coordination Network (BVCN) was to reduce some of these impacts by helping research biologists learn new skills and initiate computational projects as alternative ways to carry out their research.

Recommended citation: Tully, B. J. et al. The Bioinformatics Virtual Coordination Network: An Open-Source and Interactive Learning Environment. Frontiers in Education (2021). https://doi.org/10.3389/feduc.2021.711618 https://www.frontiersin.org/articles/10.3389/feduc.2021.711618/full

Petrobactin, a siderophore produced by Alteromonas, mediates community iron acquisition in the global ocean

Published in The ISME Journal, 2021

We identified the biosynthetic pathway for petrobactin in bacterial metagenome-assembled genomes widely distributed across the global ocean. These results improve our mechanistic understanding of the role of siderophore production in iron biogeochemical cycling in the marine environment wherein iron speciation, bioavailability, and residence time can be directly influenced by microbial activities.

Recommended citation: Manck, L. E. et al. Petrobactin, a siderophore produced by Alteromonas, mediates community iron acquisition in the global ocean. ISME J (2021). https://doi.org/10.1038/s41396-021-01065-y https://www.nature.com/articles/s41396-021-01065-y

NCBI’s Virus Discovery Codeathon: Building “FIVE” – the Federated Index of Viral Experiments API index

Published in Viruses, 2020

Viruses represent important test cases for data federation due to their genome size and the rapid increase in sequence data in publicly available databases. However, some consequences of previously decentralized (unfederated) data are lack of consensus or comparisons between feature annotations.

Recommended citation: Martí-Carreras, J. et al. NCBI’s Virus Discovery Codeathon: Building “FIVE” — The Federated Index of Viral Experiments API Index. Viruses (2020). https://doi.org/10.3390/v12121424 https://www.nature.com/articles/s41396-020-00834-5

Time-series transcriptomics from cold, oxic subseafloor crustal fluids reveals a motile, mixotrophic microbial community

Published in The ISME Journal, 2020

We used time series metagenomic and metatranscriptomic data from a low-temperature, ridge flank environment representative of the majority of global hydrothermal fluid circulation in the ocean to reconstruct microbial metabolic potential, transcript abundance, and community dynamics.

Recommended citation: Seyler, L. M., Trembath-Reichert, E., Tully, B. J. & Huber, J. A. Time-series transcriptomics from cold, oxic subseafloor crustal fluids reveals a motile, mixotrophic microbial community. ISME J (2020). https://doi.org/10.1038/s41396-020-00843-4 https://www.nature.com/articles/s41396-020-00843-4

Marine Dadabacteria exhibit genome streamlining and phototrophy-driven niche partitioning

Published in The ISME Journal, 2020

The marine Dadabacteria belong to two clades with apparent distinct ecological niches in global metagenomic data: a clade with the potential for photoheterotrophy through the use of proteorhodopsin, present predominantly in surface waters up to 100 m depth; and a clade lacking the potential for photoheterotrophy that is more abundant in the deep photic zone.

Recommended citation: Graham, E.D., Tully, B.J. Marine Dadabacteria exhibit genome streamlining and phototrophy-driven niche partitioning. ISME J (2020). https://doi.org/10.1038/s41396-020-00834-5 https://www.nature.com/articles/s41396-020-00834-5

Biases in genome reconstruction from metagenomic data

Published in PeerJ, 2020

Our results support genome reconstruction as a robust process and suggest that reconstructions determined to be >90% complete are likely to effectively represent organismal function; however, population-level genotypic heterogeneity in natural populations, such as uneven distribution of plasmids, can lead to incorrect inferences.

Recommended citation: Nelson WC, Tully BJ, Mobberley JM. 2020. Biases in genome reconstruction from metagenomic data. PeerJ 8:e10119 https://doi.org/10.7717/peerj.10119 https://peerj.com/articles/10119/

MetaSanity: an integrated microbial genome evaluation and annotation pipeline

Published in Bioinformatics, 2020

MetaSanity provides genome quality evaluation, phylogenetic assignment, as well as structural and functional annotation through a variety of integrated programs.

Recommended citation: Neely CJ, Graham ED, Tully BJ, MetaSanity: an integrated microbial genome evaluation and annotation pipeline, Bioinformatics, Volume 36, Issue 15, 1 August 2020, Pages 4341–4344, https://doi.org/10.1093/bioinformatics/btaa512 https://academic.oup.com/bioinformatics/article/36/15/4341/5840471

Genome Sequence of Mariprofundus sp. Strain EBB-1, a Novel Marine Autotroph Isolated from an Iron-Sulfur Mineral

Published in Microbiology Resource Announcements, 2019

Mariprofundus sp. strain EBB-1 was isolated from a pyrrhotite biofilm incubated in seawater from East Boothbay (ME, USA). Strain EBB-1 is an autotrophic member of the class Zetaproteobacteria with the ability to form iron oxide biominerals. Here, we present the 2.88-Mb genome sequence of EBB-1, which contains 2,656 putative protein-coding sequences.

Recommended citation: Lopez A, Albino D, Beraki S, Broomell S, Canela R, Dingmon T, Estrada S, Fernandez M, Savalia P, Nealson K, Emerson D, Barco R, Tully B, Amend J. (2019). Genome Sequence of Mariprofundus sp. Strain EBB-1, a Novel Marine Autotroph Isolated from an Iron-Sulfur Mineral. Microbiology Resource Announcements, 8(39), 1405–3. http://doi.org/10.1128/MRA.00995-19 https://mra.asm.org/content/8/39/e00995-19

NCBI’s Virus Discovery Hackathon: Engaging Research Communities to Identify Cloud Infrastructure Requirements

Published in Genes, 2019

A wealth of viral data sits untapped in publicly available metagenomic data sets when it might be extracted to create a usable index for the virological research community. We hypothesized that work of this complexity and scale could be done in a codeathon setting. Ten teams comprised of over 40 participants from six countries, assembled to create a crowd-sourced set of analysis and processing pipelines for a complex biological data set in a three-day event on the San Diego State University campus. The work yielded valuable insights into both SRA data and the cloud infrastructure required to support such efforts, revealing analysis bottlenecks and possible workarounds thereof. Here, we present the applied workflows, initial results, and lessons learned from the codeathon.

Recommended citation: Connor R, Brister R, Buchmann JP, Deboutte W, Edwards R, Martí-Carreras J, et al. (2019). NCBI’s Virus Discovery Hackathon: Engaging Research Communities to Identify Cloud Infrastructure Requirements. Genes, 10(9), 714–18. http://doi.org/10.3390/genes10090714 https://www.mdpi.com/2073-4425/10/9/714

Metabolic diversity within the globally abundant Marine Group II Euryarchaea offers insight into ecological patterns

Published in Nature Communcations, 2019

250 environmental Marine Group II Euryarchaea genomes shed light on the physiological potential and ecology of a diverse and abundant marine heterotroph.

Recommended citation: Tully BJ. (2019) Metabolic diversity within the globally abundant Marine Group II Euryarchaea offers insight into ecological patterns. Nature Communications 10:271, 1–12 https://doi.org/10.1038/s41467-018-07840-4 https://www.nature.com/articles/s41467-018-07840-4

Potential for primary productivity in a globally-distributed bacterial phototroph

Published in ISMEJ, 2018

Aerobic anoxygenic phototrophs (AAnPs) are common in marine environments and are associated with photoheterotrophic activity. To date, AAnPs that possess the potential for carbon fixation have not been identified in the surface ocean. Using the Tara Oceans metagenomic dataset, we have identified draft genomes of nine bacteria that possess the genomic potential for anoxygenic phototrophy, carbon fixation via the Calvin-Benson-Bassham cycle, and the oxidation of sulfite and thiosulfate.

Recommended citation: Graham ED, Heidelberg JF, Tully BJ. (2018) Potential for primary productivity in a globally-distributed bacterial phototroph. ISME J 350, 1–6 https://doi.org/10.1038/s41396-018-0091-3 https://www.nature.com/articles/s41396-018-0091-3

Nitrogen Cycling of Active Bacteria within Oligotrophic Sediment of the Mid-Atlantic Ridge Flank

Published in Geomicrobiology Journal, 2018

Microbial ecology within oligotrophic marine sediment is poorly understood, yet is critical for understanding geochemical cycles. Here, 16S rRNA sequences from RNA and DNA inform the structure of active and total microbial communities in oligotrophic sediment on the western flank of the Mid-Atlantic Ridge.

Recommended citation: Reese BK, Zinke LA, Sobol MS, LaRowe DE, Orcutt BN, Zhang X, Jaekel U, Wang F, Dittmar T, Defforey D, Tully B, Paytan A, Sylvan JB, Amend JP, Edwards KJ & Girguis P (2018) Nitrogen Cycling of Active Bacteria within Oligotrophic Sediment of the Mid-Atlantic Ridge Flank, Geomicrobiology Journal, https://doi.org/10.1080/01490451.2017.1392649 https://www.tandfonline.com/doi/full/10.1080/01490451.2017.1392649

The reconstruction of 2,631 draft metagenome-assembled genomes from the global oceans

Published in Scientific Data, 2018

Utilizing the large metagenomic dataset generated from 234 samples collected during the Tara Oceans circumnavigation expedition, we were able to reconstruct 2,631 draft genomes with an estimated completion of ≥50% were generated (1,491 draft genomes >70% complete; 603 genomes >90% complete).

Recommended citation: Tully BJ, Graham ED, Heidelberg JF. (2018) The reconstruction of 2,631 draft metagenome-assembled genomes from the global oceans. Scientific Data 5(170203), 1-18 https://doi.org/10.1038/sdata.2017.203 https://www.nature.com/articles/sdata2017203

A dynamic microbial community with high functional redundancy inhabits the cold, oxic subseafloor aquifer

Published in ISMEJ, 2017

Here we utilized metagenomic libraries of crustal fluid samples from North Pond, located on the flanks of the Mid-Atlantic Ridge, a site with cold, oxic subseafloor fluid circulation within the upper basement to query microbial diversity.

Recommended citation: Tully BJ, Wheat CG, Glazer BT, Huber JA. (2017) A dynamic microbial community with high functional redundancy inhabits the cold, oxic subseafloor aquifer. The ISME Journal 12, 1-16 https://doi.org/10.1038/ismej.2017.187 https://www.nature.com/articles/ismej2017187

290 metagenome-assembled genomes from the Mediterranean Sea: a resource for marine microbiology

Published in PeerJ, 2017

Utilizing several size fractions from the samples originating in the Mediterranean Sea, we have used current assembly and binning techniques to reconstruct 290 putative draft metagenome-assembled bacterial and archaeal genomes.

Recommended citation: Tully BJ, Sachdeva R, Graham ED, Heidelberg JF. (2017) 290 metagenome-assembled genomes from the Mediterranean Sea: a resource for marine microbiology. PeerJ 5:e3558 https://doi.org/10.7717/peerj.3558 https://peerj.com/articles/3558/

BinSanity: unsupervised clustering of environmental microbial assemblies using coverage and affinity propagation

Published in PeerJ, 2017

We are introducing a new binning method, BinSanity, that utilizes the clustering algorithm affinity propagation (AP), to cluster assemblies using coverage with compositional based refinement (tetranucleotide frequency and percent GC content) to optimize bins containing multiple source organisms.

Recommended citation: Graham, E. D., Heidelberg, J. F., & Tully, B. J. (2017). BinSanity: unsupervised clustering of environmental microbial assemblies using coverage and affinity propagation. PeerJ, 5(Part B), e3035–19. http://doi.org/10.7717/peerj.3035 https://peerj.com/articles/3035/

Potential Mechanisms for Microbial Energy Acquisition in Oxic Deep-Sea Sediments

Published in Applied and environmental microbiology, 2016

The South Pacific Gyre (SPG) possesses the lowest rates of sedimentation, surface chlorophyll concentration, and primary productivity in the global oceans. As a direct result, deep-sea sediments are thin and contain small amounts of labile organic carbon. It was recently shown that the entire SPG sediment column is oxygenated and may be representative of up to a third of the global marine environment. To understand the microbial processes that contribute to the removal of the labile organic matter at the water-sediment interface, a sediment sample was collected and subjected to metagenomic sequencing and analyses.

Recommended citation: Tully, B. J., & Heidelberg, J. F. (2016). Potential Mechanisms for Microbial Energy Acquisition in Oxic Deep-Sea Sediments. Applied and Environmental Microbiology, 82(14), 4232–4243. http://doi.org/10.1128/AEM.01023-16 http://aem.asm.org/content/82/14/4232.short

A distinct and active bacterial community in cold oxygenated fluids circulating beneath the western flank of the Mid-Atlantic ridge

Published in Scientific Reports, 2016

The rock-hosted, oceanic crustal aquifer is one of the largest ecosystems on Earth, yet little is known about its indigenous microorganisms. Here we provide the first phylogenetic and functional description of an active microbial community residing in the cold oxic crustal aquifer.

Recommended citation: Meyer, J. L., Jaekel, U., Tully, B. J., Glazer, B. T., Wheat, C. G., Lin, H.-T., et al. (2016). A distinct and active bacterial community in cold oxygenated fluids circulating beneath the western flank of the Mid-Atlantic ridge. Scientific Reports, 6, 22541. http://doi.org/10.1038/srep22541 http://www.nature.com/articles/srep22541?WT.feed_name=subjects_ocean-sciences

De novo sequences of Haloquadratum walsbyi from Lake Tyrrell, Australia, reveal a variable genomic landscape

Published in Archaea, 2015

Hypersaline systems near salt saturation levels represent an extreme environment, in which organisms grow and survive near the limits of life. One of the abundant members of the microbial communities in walsbyi. Utilizing a short-read metagenome from Lake Tyrrell, a hypersaline ecosystem in hypersaline systems is the square archaeon, Haloquadratum Victoria, Australia, we performed a comparative genomic analysis of H. walsbyi to better understand the extent of variation between strains/subspecies.

Recommended citation: Tully, B. J., Emerson, J. B., Andrade, K., Brocks, J. J., Allen, E. E., Banfield, J. F., & Heidelberg, K. B. (2015). De NovoSequences of Haloquadratum walsbyifrom Lake Tyrrell, Australia, Reveal a Variable Genomic Landscape. Archaea, 2015(4), 1–12. http://doi.org/10.1155/2015/875784 https://www.hindawi.com/journals/archaea/2015/875784/

Comparative genomics of planktonic Flavobacteriaceae from the Gulf of Maine using metagenomic data

Published in Microbiome, 2014

The Gulf of Maine is an important biological province of the Northwest Atlantic with high productivity year round. From an environmental Sanger-based metagenome, sampled in summer and winter, we were able to assemble and explore the partial environmental genomes of uncultured members of the class Flavobacteria. Each of the environmental genomes represents organisms that compose less than 1% of the total microbial metagenome.

Recommended citation: Tully, B. J., Sachdeva, R., Heidelberg, K. B., & Heidelberg, J. F. (2014). Comparative genomics of planktonic Flavobacteriaceae from the Gulf of Maine using metagenomic data, Microbiome, 2(1), 1–14. http://doi.org/10.1186/2049-2618-2-34 https://microbiomejournal.biomedcentral.com/articles/10.1186/2049-2618-2-34

Microbial communities associated with ferromanganese nodules and the surrounding sediments

Published in Frontiers in microbiology, 2013

The formation and maintenance of deep-sea ferromanganese/polymetallic nodules still remains a mystery 140 years after their discovery. The wealth of rare metals concentrated in these nodules has spurred global interest in exploring the mining potential of these resources. The prevailing theory of abiotic formation has been called into question and the role of microbial metabolisms in nodule development is now an area of active research. To understand the community structure of microbes associated with nodules and their surrounding sediment, we performed targeted sequencing of the V4 hypervariable region of the 16S rRNA gene from three nodules collected from the central South Pacific.

Recommended citation: Tully, B. J., & Heidelberg, J. F. (2013). Microbial communities associated with ferromanganese nodules and the surrounding sediments. Frontiers in Microbiology, 4, 161. http://doi.org/10.3389/fmicb.2013.00161 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3691505/

Prospects for the study of evolution in the deep biosphere

Published in Frontiers in microbiology, 2012

Microbial biogeography and adaptation has been examined in many different environments. Here we argue that the deep biosphere is a unique environment for the study of evolution and list specific factors that can be considered and where the studies may be performed.

Recommended citation: Biddle, J. F., Sylvan, J. B., Brazelton, W. J., Tully, B. J., Edwards, K. J., Moyer, C. L., et al. (2011). Prospects for the study of evolution in the deep biosphere. Frontiers in Microbiology, 2, 285. http://doi.org/10.3389/fmicb.2011.00285 http://journal.frontiersin.org/article/10.3389/fmicb.2011.00285/full

Metagenomic analysis of a complex marine planktonic thaumarchaeal community from the Gulf of Maine

Published in Environmental microbiology, 2012

Thaumarchaea, which represent as much as 20% of prokaryotic biomass in the open ocean, have been linked to environmentally relevant biogeochemical processes, such as ammonia oxidation (nitrification) and inorganic carbon fixation. We have used culture-independent methods to study this group because current cultivation limitations have proved a hindrance in studying these organisms.

Recommended citation: Tully, B. J., Nelson, W. C., & Heidelberg, J. F. (2011). Metagenomic analysis of a complex marine planktonic thaumarchaeal community from the Gulf of Maine. Environmental Microbiology, 14(1), 254–267. http://doi.org/10.1111/j.1462-2920.2011.02628.x http://onlinelibrary.wiley.com/doi/10.1111/j.1462-2920.2011.02628.x/full

Dr. Benjamin Tully

Publications