Microbial 'omics

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Single-amino acid variants reveal evolutionary processes that shape the biogeography of a global SAR11 subclade.

Delmont, T. O., Kiefl, E., Kilinc, O., Esen, Ö. C., Uysal, I., Rappé, M. S., Giovannoni, S., and Eren, A. M.
- A study that introduces 'single-amino acid variants' (SAAVs) and demonstrates the use of SAAVs to tease apart evolutionary processes that shape the biogeography and genomic heterogeneity within a SAR11 population through metagenomics.
- A first attempt to link population genetics and the predicted protein structures to explore in silico the intersection beetween protein biochemistry and evolutionary processes acting on an environmental microbe.
- An application of metapangenomics to define subclades of SAR11 based on gene content and ecology.
- Reproducible bioinformatics workflow is here. Reviewer criticism and our responses are also available.
eLife. 8:e46497

Composite metagenome-assembled genomes reduce the quality of public genome repositories.

Shaiber, A., and Eren, A. M.
- A letter that stresses that the composite metagenome-assembled genomes influence phylogenomic, pangenomic, and ecological insights (peer reviews and responses).
- A reproducible workflow to detail the steps of genome refinement and make available the refined versions of some key genomes.
mBio. 10(3) e00725-19

The Wolbachia mobilome in Culex pipiens includes a putative plasmid.

Reveillaud, R., Bordenstein, S. R., Cruaud, C., Shaiber, A., Esen, Ö. C., O. C., Weill, M., Makoundou, P., Lolans, K., Watson, A. R., Rakotoarivony, I., Bordenstein, S. R., and Eren, A. M.
- The first report of a Wolbachia plasmid through genome-resolved metagenomics on microsurgically removed individual mosquito ovary samples (peer reviews and responses).
- Yet another application of metapangenomics and an applicatoin of minION long-read sequencing on extremely low-biomass samples.
- Reproducible bioinformatics workflow with all data items, a 'behind the paper' blog post by Julie Reveillaud, and a press release from the Marine Biological Laboratory.
Nature Communications. 10:1051

Genome-resolved insights into a novel Spiroplasma symbiont of the Wheat Stem Sawfly.

Yeoman, C. J., Brutscher, L. M., Esen, Ö. C., Ibaoglu, F., Fowler, C., Eren, A. M., Wanner, K., and Weaver, D. K.
- A study that uses (1) genome-resolved metagenomics to reconstruct a population genome from fly metagenomes that resolves to the genus Spiroplasma, (2) pangenomics to put this genome in the context of other Spiroplasma genomes, (3) phylogenomics to infer ancestral relationships between Spiroplasma genomes, and (4) includes an ANI-based distance estimation between all genomes for comprehensive reporting.
- It is a particularly good example that demonstrates how pangenomics can reveal appropriate targets for high-resolution phylogenomics.
- A fully reproducible bioinformatics workflow for this multi'omics analysis is here. Anvi'o databases to interactively reproduce and explore the Spiroplasma pangenome is also available.
PeerJ. 7:e7548

Global phylogeography and ancient evolution of the widespread human gut virus crAssphage.

Edwards, R. A., Vega, A. A., Norman, H. M., Ohaeri, M., Levi, K., Dinsdale, E. A., Cinek, O., Aziz, R. K., McNair, K., Barr, J. J., Bibby, K., Brouns, SJJ., Cazares, A., deJonge, P. A., Desnues, C., Díaz Muñoz, S. L., Fineran, P. C., Kurilshikov, A., Lavigne, R., Mazankova, K., McCarthy, D. T., Nobrega, F. L., Reyes Muñoz, A., Tapia, G., Trefault, N., Tyakht, A. V., Vinuesa, P., Wagemans, J., Zhernakova, A., Aarestrup, F. M., Ahmadov, G., Alassaf, A., Anton, J., Asangba, A., Billings, E. K., Cantu, V. A., Carlton, J. M., Cazares, D., Cho, G. S., Condeff, T., Cortés, P., Cranfield, M., Cuevas, D. A., De la Iglesia, R., Decewicz, P., Doane, M. P., Dominy, N. J., Dziewit, L., Elwasila, B. M., Eren, A. M., Franz, C., Fu, J., Garcia-Aljaro, C., Ghedin, E., Gulino, K. M., Haggerty, J. M., Head, S. R., Hendriksen, R. S., Hill, C., Hyöty, H., Ilina, E. N., Irwin, M. T., Jeffries, T. C., Jofre, J., Junge, R. E., Kelley, S. T., Khan Mirzaei, M., Kowalewski, M., Kumaresan, D., Leigh, S. R., Lipson, D., Lisitsyna, E. S., Llagostera, M., Maritz, J. M., Marr, L. C., McCann, A., Molshanski-Mor, S., Monteiro, S., Moreira-Grez, B., Morris, M., Mugisha, L., Muniesa, M., Neve, H., Nguyen, N. P., Nigro, O. D., Nilsson, A. S., O'Connell, T., Odeh, R., Oliver, A., Piuri, M., Prussin Ii, A. J., Qimron, U., Quan, Z. X., Rainetova, P., Ramírez-Rojas, A., Raya, R., Reasor, K., Rice, GAO., Rossi, A., Santos, R., Shimashita, J., Stachler, E. N., Stene, L. C., Strain, R., Stumpf, R., Torres, P. J., Twaddle, A., Ugochi Ibekwe, M., Villagra, N., Wandro, S., White, B., Whiteley, A., Whiteson, K. L., Wijmenga, C., Zambrano, M. M., Zschach, H., and Dutilh, B. E.
- A monumental effort lead by Rob Edwards and Bas Dutilh to explore with the help of 114 scientists from around the world the global phylogeorgraphy and evolution of crAssphage, one of the most numerous viruses in the human gut that infect bacteria.
- A curated list of press coverage of this study is available on Rob Edwards' web site.
Nature Microbiology. ahead of print

Co-occurring genomic capacity for anaerobic methane and dissimilatory sulfur metabolisms discovered in the Korarchaeota.

McKay, L. J., Dlakić, M., Fields, M. W., Delmont, T. O., Eren, A. M., Jay, Z. J., Klingelsmith, K. B., Rusch, D. B., and Inskeep, W. P.
- Yesllowstone National Park, archaeal evolution, genome-resolved metagenomics, phylogenomics, and pangenomics (cool stuff all over).
- First description of a microbial population with both anaerobic methane and dissimilatory sulfur metabolisms.
- A news article by Montana State University with the photographs of cools scientists: An organism in Yellowstone hot spring potentially linked to earliest life on Earth"
Nature Microbiology. 2058-5276



Microbiome characterization by high-throughput transfer RNA sequencing and modification analysis.

Schwartz, M. H., Wang, H., Pan, J. N., Clark. W. C., Cui, S., Eckwahl, M. J., Pan, D. W., Parisien, M., Owens, S. M., Cheng, B. L., Martinez, K., Xu, J., Chang, E. B., Pan, T., and Eren, A. M.
- First application of tRNA sequencing to microbiomes (peer reviews and responses).
- tRNA-seq distinguishes high-fat- and low-fat-fed mice in a comparable fashion to 16S rRNA gene amplicons, reveals taxon- and diet-dependent variations in tRNA modifications, and provides in situ insights into tRNA gene expression dynamics and post-transcriptional modifications.
- "New RNA sequencing strategy provides insight into microbiomes", by Matt Wood.
- "RNA sequencing offers novel insights into the microbiome", by Liji Thomas, MD, and Kate Anderton, B.Sc.
Nature Communications. 9:5353

Nitrogen-fixing populations of Planctomycetes and Proteobacteria are abundant in the surface ocean metagenomes.

Delmont, T. O., Quince, C., Shaiber, A., Esen, Ö. C., Lee, S. T. M., Rappé, M. S., McLellan, S. L., Lücker, S., and Eren, A. M.
- First genomic evidence for abundant and widespread non-cyanobacterial nitrogen-fixing populations in the surface ocean.
- Nearly 1,000 non-redundant, high-quality bacterial, archaeal, and eukaryotic population genomes from TARA Oceans metagenomes.
- A "behind the paper" blog post by Meren, a press release by the MBL, and an extensive description of the bioinformatics workflow.
Nature Microbiology. 3:804–813

Linking pangenomes and metagenomes: the Prochlorococcus metapangenome.

Delmont, T. O., and Eren, A. M.
- A big-data study in which a pangenome of 31 Prochlorococcus isolates meets 31 billion Tara Oceans metagenomic sequences (Peer-review history).
- Metapangenomes reveal to what extent genes that may be linked to the ecology and fitness of microbes are conserved within a phylogenetic clade.
- Reproducible bioinformatics workflow.
PeerJ. 6:e4320

Transcriptome-wide reprogramming of N6-methyladenosine modification by the mouse microbiome.

Wang, X., Li, Y., Chen, W., Shi, H., Eren, A. M., Morozov, A., He, C., Luo, G. Z., and Pan, T.
- N6-methyladenosine (m6A) is the most abundant mesenger RNA modification in mammalian cells, occurring at ~3 modified adenosine residues per transcript.
- Using liquid chromatography/mass spectrometry, this study shows differential occurrence of m6A modifications in brain, liver, and intestinal cells between germ-free and conventional mice, demonstrating that the microbiome has a strong effect on host m6A mRNA modification.
Cell Research. 0:1-4

Gut microbes contribute to variation in solid organ transplant outcomes in mice.

McIntosh, C. M., Chen, L., Shaiber, A., Eren, A. M., and Alegre, M. L.
- Two groups of genetically identical mice with different microbial community structures differ in their response to skin transplants from genetically identical sources: one group rejects the skin faster than the other.
- Transferring poop from slow-rejecting mice into fast-rejecting mice turns fast-rejecting mice into slow-rejecting mice.
- These suggest that differences in 'resident microbiome' in healthy individuals may contribute to interpersonal variability in graft outcomes, and fecal microbiota transplantation may play a therapeutic role to reverse that phenotype.
- Basically, "we do not have a mechanistic understanding, but this is definitely very interesting".
Microbiome. 6:96

Microbial signals drive pre-leukaemic myeloproliferation in a Tet2-deficient host.

Meisel, M., Hinterleitner, R., Pacis, A., Chen, L., Earley, Z. M., Mayassi, T., Pierre, J. F., Ernest, J. D., Galipeau, H. J., Thuille, N., Bouziat, R., Buscarlet, M., Ringus, D. L., Wang, Y., Li, Y., Dinh, V., Kim, S. M., McDonald, B. D., Zurenski, M. A., Musch, M. W., Furtado, G. C., Lira, S. A., Baier, G., Chang, E. B., Eren, A. M., Weber, C. R., Busque, L., Godley, L. A., Verdú, E. F., Barreiro, L. B., and Jabri, B.
- TET2 deficiency ➡️ deteriorating small intestinal barrier ➡️ bacterial translocation ➡️ incrased IL-6 signalling ➡️ pre-leukemic myeloproliferation (a leukemia precursor).
- ScienceDaily: Under certain conditions, bacterial signals set the stage for leukemia.
Nature. 557:580–584



Tracking microbial colonization in fecal microbiota transplantation experiments via genome-resolved metagenomics.

Lee, S. T. M., Kahn, S. A., Delmont, T. O., Shaiber, A., Esen, Ö. C., Hubert, N. A., Morrison, H. G., Antonopoulos, D. A., Rubin, D. T., and Eren, A. M.
- An FMT study with metagenome-assembled genomes (see public data).
- Bacteroidales: high-colonization rate. Clostridiales: low colonization rate. Colonization success is negatively correlated with the number of genes related to sporulation.
- MAGs with the same taxonomy showed different colonization properties, highlighting the importance of high-resolution analyses.
- Populations colonized both recipients were also prevalent in the HMP cohort (and the ones that did not, distribute sporadically across the HMP cohort).
Microbiome. 5:50

Simulations predict microbial responses in the environment? This environment disagrees retrospectively.

Delmont, T. O., and Eren, A. M.
- A letter that re-analyzes some of the findings published in Hu et al.
- Here is a rebuttal from Probst et al. challenging our findings in this letter.
- Here is our response to Probst et al., and the recovery of DWH O. Desum v2.
Proc Natl Acad Sci U S A. 114(43):E8947-E8949

Genomic variation in microbial populations inhabiting the marine subseafloor at deep-sea hydrothermal vents.

Anderson, R. E., Reveillaud, J., Reddington, E., Delmont, T. O., Eren, A. M., McDermott, J. M., Seewald, J. S., and Huber, J. A. Nature Communications. 8:1114

Recurrent patterns of microdiversity in a temperate coastal marine environment.

Chafee, M., Fernàndez-Guerra, A., Buttigieg, P. L., Gerdts, G., Eren, A. M., Teeling, H., and Amann, R. I. ISME J. 12, 237–252

DESMAN: a new tool for de novo extraction of strains from metagenomes.

Quince, C., Delmont, T. O., Raguideau, S., Alneberg, J., Darling, A. E., Collins, G., and Eren, A. M. Genome Biology. 18:181

Minimum information about a single amplified genome (MISAG) and a metagenome-assembled genome (MIMAG) of bacteria and archaea.

Bowers, R. M., Kyrpides, N. C., Stepanauskas, R., Harmon-Smith, M., Doud, D., Reddy, TBK., Schulz, F., Jarett, J., Rivers, A. R., Eloe-Fadrosh, E. A., Tringe, S. G., Ivanova, N. N., Copeland, A., Clum, A., Becraft, E. D., Malmstrom, R. R., Birren, B., Podar, M., Bork, P., Weinstock, G. M., Garrity, G. M., Dodsworth, J. A., Yooseph, S., Sutton, G., Glöckner, F. O., Gilbert, J. A., Nelson, W. C., Hallam, S. J., Jungbluth, S. P., Ettema, G., Tighe, S., Konstantinidis, K. T., Liu, W., Baker, B. J., Rattei, T., Eisen, J. A., Hedlund, B., McMahon, K. D., Fierer, N., Knight, R., Finn, R., Cochrane, G., Karsch-Mizrachi, I., Tyson, G. W., Rinke, C., Lapidus, A., Meyer, F., Yilmaz, P., Parks, D. H., Eren, A. M., Schriml, L., Banfield, J. F., Hugenholtz, P., Woyke, T. Nature Biotechnology. 35:725–731

Peripartum Antibiotics Promote Gut Dysbiosis, Loss of Immune Tolerance, and Inflammatory Bowel Disease in Genetically Prone Offspring.

Miyoshi, J., Bobe, A. M., Miyoshi, S., Huang, Y., Hubert, N., Delmont, T. O., Eren, A. M., Leone, V., and Chang, E. B.
- Antibiotics during pregnancy promote offspring gut dysbiosis, immune dysfunction, and IBD.
- Antibiotics given after the developmental period do not increase IBD.
- Antibiotic-perturbed maternal microbiota likely contribute to neonatal gut dysbiosis.
- Press release.
Cell Reports. 20:2

Early Transcriptomic Changes in the Ileal Pouch Provide Insight into the Molecular Pathogenesis of Pouchitis and Ulcerative Colitis.

Huang, Y., Dalal, S., Antonopoulos, D., Hubert, N., Raffals, L. H., Dolan, K., Weber, C., Messer, J. S., Jabri, B., Bendelac, A., Eren, A. M., Rubin, D. T., Sogin, M. L., and Chang, E. B. Inflammatory Bowel Disiseases. 23(3):366-378

A Few Pseudomonas Oligotypes Dominate in the Meat and Dairy Processing Environment.

Stellato, G., Utter, D. R., Voorhis, A., De Angelis, M., Eren, A. M., and Ercolini, D. Front Microbiol. 8:264



Identifying contamination with advanced visualization and analysis practices: metagenomic approaches for eukaryotic genome assemblies.

Delmont, T. O., and Eren, A. M.
- A holistic approach to visualize and curate genomic and metagenomic assemblies.
- A re-analysis of the first released Tardigrade genome reveals a likely symbiont among other contaminants.
- A practical approach to estimate the number bacterial genomes in an assembly.
PeerJ. 4:e1839

Patient-specific Bacteroides genome variants in pouchitis.

Vineis, J. H., Ringus, D. L., Morrison, H. G., Delmont, T. O., Dalal, S., Raffals, L. H., Antonopoulos, D. A., Rubin, D. T., Eren, A. M., Chang, E. B., and Sogin, M. L mBio. 7(6):e01713-16

New insights into microbial ecology through subtle nucleotide variation.

Eren, A. M., Sogin, M. L., and Maignien, L. Front Microbiol. 7:1318

Millions of reads, thousands of taxa: microbial community structure and associations analyzed via marker genes.

Bálint, M., Bahram, M., Eren, A. M., Faust, K., Fuhrman, J. A., Lindahl, B., O'Hara, R. B., Öpik, M., Sogin, M. L., Unterseher, M., and Tedersoo, L. FEMS Microbiology Reviews. na:na

Bacterial communities in penile skin, male urethra, and vaginas of heterosexual couples with and without bacterial vaginosis.

Zozaya, M., Ferris, M. J., Siren, J. D., Lillis, R., Myers, L., Nsuami, M. J., Eren, A. M., Brown, J., Taylor, C. M., and Martin, D. H. Microbiome. 4:16



Anvi’o: An advanced analysis and visualization platform for ‘omics data.

Eren, A. M., Esen, Ö. C., Quince, C., Vineis, J. H., Morrison, H. G., Sogin, M. L., and Delmont, T. O.
- The methods paper for anvi'o.
- Binning, and single-nucleotide variant analysis of a human gut time series metagenome.
- Re-analysis of cultivar genomes, metagenomes, and metatranscriptomes associated with the Deepwater Horizon oil spill.
PeerJ. 6:358

Comparison of sewage and animal fecal microbiomes using oligotyping reveals potential human fecal indicators in multiple taxonomic groups.

Fisher, J. C., Eren, A. M., Green, H. C., Shanks, O. C., Morrison, H. G., Vineis, J. H., Sogin, M. L., and McLellan, S. L. Appl Environ Microbiol. 81, 7023–7033

Reconstructing Rare Soil Microbial Genomes using in situ Enrichments and Metagenomics.

Delmont, T. O., Eren, A. M., Maccario, L., Prestat, E., Esen, Ö. C., Pelletier, E., LePaslier, D., Simonet, P., and Vogel, T.
- Application of in situ enrichments to shape the diversity of complex metagenomes prior to sequencing.
- The first successful attempt to assemble multiple near-complete bacterial genomes directly from a soil sample.
- The abundance of reconstructed genomes ranged from rare (<0.0001%) to relatively abundant (>0.01%) in pristine soil metagenomes.
Front Microbiol. 6:358

A single genus in the gut microbiome reflects host preference and specificity.

Eren, A. M., Sogin, M. L., Morrison, H. G., Vineis, J. H., Fisher, J. C., Newton, R. J., and McLellan, S. L. ISME J. 9(1), 90-100

Minimum entropy decomposition: Unsupervised oligotyping for sensitive partitioning of high-throughput marker gene sequences.

Eren, A. M., Morrison, H. G., Lescault, P. J., Reveillaud, J., Vineis, J. H., and Sogin, M. L. ISME J. 9, 968-79

Sewage reflects the microbiomes of human populations.

Newton, R. J., McLellan, S. L., Dila, D. K., Vineis, J. H., Morrison, H. G., Eren, A. M., and Sogin, M. L. mBio. 6:2

Extensive Modulation of the Fecal Metagenome in Children With Crohn's Disease During Exclusive Enteral Nutrition.

Quince, C., Ijaz, U. Z., Loman, N., Eren, A. M., Saulnier, D., Russell, J., Haig, S. J., Calus, S. T., Quick, J., Barclay, A., Bertz, M., Hansen, R., McGrogan, P., Russel, K. R., Edwards, C. A., and Gerasimidis, K. Am J Gastroenterol. 110:1718–1729



Oligotyping analysis of the human oral microbiome.

Eren, A. M., Borisy, G. G., Huse, S. M., and Mark Welch, J. L. Proc Natl Acad Sci U S A. 111(28), E2875-84

DRISEE overestimates errors in metagenomic sequencing data.

Eren, A. M., Morrison, H. G., Huse, S. M., and Sogin, M. L. Brief Bioinform. 15(5), 783-7

Humpback whale populations share a core skin bacterial community: towards a health index for marine mammals?

Apprill, A., Robbins, J., Eren, A. M., Pack, A. A., Reveillaud, J., Mattila, D., Moore, M., Niemeyer, M., Moore, K. M., and Mincer, T. J. PLoS One. 9(3), e90785

Ecological succession and stochastic variation in the assembly of Arabidopsis thaliana phyllosphere communities.

Maignien, L., DeForce, E. A., Chafee, M. E., Eren, A. M., and Simmons, S. L. MBio. 5(1), e00682-13

SeaBase: a multispecies transcriptomic resource and platform for gene network inference.

Fischer, A. H., Mozzherin, D., Eren, A. M., Lans, K. D., Wilson, N., Cosentino, C., and Smith, J. Integr Comp Biol. 54(2), 250-63

VAMPS: a website for visualization and analysis of microbial population structures.

Huse, S. M., Mark Welch, D. B., Voorhis, A., Shipunova, A., Morrison, H. G., Eren, A. M., and Sogin, M. L. BMC Bioinformatics. 15(1), 41

Blautia and Prevotella sequences distinguish human and animal fecal pollution in Brazil surface waters.

Koskey, A. M., Fisher, J. C., Eren, A. M., Ponce-Terashima, R., Reis, M. G., Blanton, R. E., and McLellan, S. L. Environ Microbiol Rep. 6(6), 696-704

Discovering new indicators of fecal pollution.

McLellan, S. L., and Eren, A. M. Trends Microbiol. 22(12), 697-706

Host-specificity among abundant and rare taxa in the sponge microbiome.

Reveillaud, J., Maignien, L., Eren, A. M., Huber, J. A., Apprill, A., Sogin, M. L., and Vanreusel, A. ISME J. 8(6), 1198-209

Dynamics of tongue microbial communities with single-nucleotide resolution using oligotyping.

Mark Welch, J. L., Utter, D. R., Rossetti, B. J., Mark Welch, D. B., Eren, A. M., and Borisy, G. G. Front Microbiol. 5:568



Oligotyping: Differentiating between closely related microbial taxa using 16S rRNA gene data.

Eren, A. M., Maignien, L., Sul, W. J., Murphy, L. G., Grim, S. L., Morrison, H. G., and Sogin, M. L. Methods Ecol Evol. 4(12)

A filtering method to generate high quality short reads using illumina paired-end technology.

Eren, A. M., Vineis, J. H., Morrison, H. G., and Sogin, M. L. PLoS One. 8(6), e66643

Histamine-2 receptor blockers alter the fecal microbiota in premature infants.

Gupta, R. W., Tran, L., Norori, J., Ferris, M. J., Eren, A. M., Taylor, C. M., Dowd, S. E., and Penn, D. J Pediatr Gastroenterol Nutr. 56(4), 397-400

Sewage reflects the distribution of human faecal Lachnospiraceae.

McLellan, S. L., Newton, R. J., Vandewalle, J. L., Shanks, O. C., Huse, S. M., Eren, A. M., and Sogin, M. L. Environ Microbiol. 15(8), 2213-27

Multiphasic analysis of the temporal development of the distal gut microbiota in patients following ileal pouch anal anastomosis.

Young, V. B., Raffals, L. H., Huse, S. M., Vital, M., Dai, D., Schloss, P. D., Brulc, J. M., Antonopoulos, D. A., Arrieta, R. L., Kwon, J. H., Reddy, K. G., Hubert, N. A., Grim, S. L., Vineis, J. H., Dalal, S., Morrison, H. G., Eren, A. M., Meyer, F., Schmidt, T. M., Tiedje, J. M., Chang, E. B., and Sogin, M. L. Microbiome. 1(1), 9