Bacteroidales species in the human gut are a reservoir of antibiotic resistance genes regulated by invertible promoters View Full Text


Ontology type: schema:ScholarlyArticle      Open Access: True


Article Info

DATE

2022-01-10

AUTHORS

Wei Yan, A. Brantley Hall, Xiaofang Jiang

ABSTRACT

Antibiotic-resistance genes (ARGs) regulated by invertible promoters can mitigate the fitness cost of maintaining ARGs in the absence of antibiotics and could potentially prolong the persistence of ARGs in bacterial populations. However, the origin, prevalence, and distribution of these ARGs regulated by invertible promoters remains poorly understood. Here, we sought to assess the threat posed by ARGs regulated by invertible promoters by systematically searching for ARGs regulated by invertible promoters in the human gut microbiome and examining their origin, prevalence, and distribution. Through metagenomic assembly of 2227 human gut metagenomes and genomic analysis of the Unified Human Gastrointestinal Genome (UHGG) collection, we identified ARGs regulated by invertible promoters and categorized them into three classes based on the invertase-regulating phase variation. In the human gut microbiome, ARGs regulated by invertible promoters are exclusively found in Bacteroidales species. Through genomic analysis, we observed that ARGs regulated by invertible promoters have convergently originated from ARG insertions into glycan-synthesis loci that were regulated by invertible promoters at least three times. Moreover, all three classes of invertible promoters regulating ARGs are located within integrative conjugative elements (ICEs). Therefore, horizontal transfer via ICEs could explain the wide taxonomic distribution of ARGs regulated by invertible promoters. Overall, these findings reveal that glycan-synthesis loci regulated by invertible promoters in Bacteroidales species are an important hotspot for the emergence of clinically-relevant ARGs regulated by invertible promoters. More... »

PAGES

1

Identifiers

URI

http://scigraph.springernature.com/pub.10.1038/s41522-021-00260-1

DOI

http://dx.doi.org/10.1038/s41522-021-00260-1

DIMENSIONS

https://app.dimensions.ai/details/publication/pub.1144548355

PUBMED

https://www.ncbi.nlm.nih.gov/pubmed/35013297


Indexing Status Check whether this publication has been indexed by Scopus and Web Of Science using the SN Indexing Status Tool
Incoming Citations Browse incoming citations for this publication using opencitations.net

JSON-LD is the canonical representation for SciGraph data.

TIP: You can open this SciGraph record using an external JSON-LD service: JSON-LD Playground Google SDTT

[
  {
    "@context": "https://springernature.github.io/scigraph/jsonld/sgcontext.json", 
    "about": [
      {
        "id": "http://purl.org/au-research/vocabulary/anzsrc-for/2008/06", 
        "inDefinedTermSet": "http://purl.org/au-research/vocabulary/anzsrc-for/2008/", 
        "name": "Biological Sciences", 
        "type": "DefinedTerm"
      }, 
      {
        "id": "http://purl.org/au-research/vocabulary/anzsrc-for/2008/0604", 
        "inDefinedTermSet": "http://purl.org/au-research/vocabulary/anzsrc-for/2008/", 
        "name": "Genetics", 
        "type": "DefinedTerm"
      }, 
      {
        "inDefinedTermSet": "https://www.nlm.nih.gov/mesh/", 
        "name": "Anti-Bacterial Agents", 
        "type": "DefinedTerm"
      }, 
      {
        "inDefinedTermSet": "https://www.nlm.nih.gov/mesh/", 
        "name": "Drug Resistance, Microbial", 
        "type": "DefinedTerm"
      }, 
      {
        "inDefinedTermSet": "https://www.nlm.nih.gov/mesh/", 
        "name": "Gastrointestinal Microbiome", 
        "type": "DefinedTerm"
      }, 
      {
        "inDefinedTermSet": "https://www.nlm.nih.gov/mesh/", 
        "name": "Humans", 
        "type": "DefinedTerm"
      }, 
      {
        "inDefinedTermSet": "https://www.nlm.nih.gov/mesh/", 
        "name": "Metagenomics", 
        "type": "DefinedTerm"
      }, 
      {
        "inDefinedTermSet": "https://www.nlm.nih.gov/mesh/", 
        "name": "Phase Variation", 
        "type": "DefinedTerm"
      }
    ], 
    "author": [
      {
        "affiliation": {
          "alternateName": "National Library of Medicine, National Institutes of Health, Bethesda, Maryland, USA", 
          "id": "http://www.grid.ac/institutes/grid.280285.5", 
          "name": [
            "National Library of Medicine, National Institutes of Health, Bethesda, Maryland, USA"
          ], 
          "type": "Organization"
        }, 
        "familyName": "Yan", 
        "givenName": "Wei", 
        "id": "sg:person.012071475727.80", 
        "sameAs": [
          "https://app.dimensions.ai/discover/publication?and_facet_researcher=ur.012071475727.80"
        ], 
        "type": "Person"
      }, 
      {
        "affiliation": {
          "alternateName": "Center for Bioinformatics and Computational Biology, University of Maryland, College Park, Maryland, USA", 
          "id": "http://www.grid.ac/institutes/grid.164295.d", 
          "name": [
            "Department of Cell Biology and Molecular Genetics, University of Maryland, College Park, Maryland, USA", 
            "Center for Bioinformatics and Computational Biology, University of Maryland, College Park, Maryland, USA"
          ], 
          "type": "Organization"
        }, 
        "familyName": "Hall", 
        "givenName": "A. Brantley", 
        "id": "sg:person.01024545742.89", 
        "sameAs": [
          "https://app.dimensions.ai/discover/publication?and_facet_researcher=ur.01024545742.89"
        ], 
        "type": "Person"
      }, 
      {
        "affiliation": {
          "alternateName": "National Library of Medicine, National Institutes of Health, Bethesda, Maryland, USA", 
          "id": "http://www.grid.ac/institutes/grid.280285.5", 
          "name": [
            "National Library of Medicine, National Institutes of Health, Bethesda, Maryland, USA"
          ], 
          "type": "Organization"
        }, 
        "familyName": "Jiang", 
        "givenName": "Xiaofang", 
        "id": "sg:person.01227353652.96", 
        "sameAs": [
          "https://app.dimensions.ai/discover/publication?and_facet_researcher=ur.01227353652.96"
        ], 
        "type": "Person"
      }
    ], 
    "citation": [
      {
        "id": "sg:pub.10.1038/nrmicro2319", 
        "sameAs": [
          "https://app.dimensions.ai/details/publication/pub.1000198743", 
          "https://doi.org/10.1038/nrmicro2319"
        ], 
        "type": "CreativeWork"
      }, 
      {
        "id": "sg:pub.10.1186/1471-2105-5-113", 
        "sameAs": [
          "https://app.dimensions.ai/details/publication/pub.1040413794", 
          "https://doi.org/10.1186/1471-2105-5-113"
        ], 
        "type": "CreativeWork"
      }, 
      {
        "id": "sg:pub.10.1038/s41587-020-0603-3", 
        "sameAs": [
          "https://app.dimensions.ai/details/publication/pub.1129483269", 
          "https://doi.org/10.1038/s41587-020-0603-3"
        ], 
        "type": "CreativeWork"
      }, 
      {
        "id": "sg:pub.10.1038/nmeth.1923", 
        "sameAs": [
          "https://app.dimensions.ai/details/publication/pub.1006541515", 
          "https://doi.org/10.1038/nmeth.1923"
        ], 
        "type": "CreativeWork"
      }, 
      {
        "id": "sg:pub.10.1007/bf00383309", 
        "sameAs": [
          "https://app.dimensions.ai/details/publication/pub.1016899890", 
          "https://doi.org/10.1007/bf00383309"
        ], 
        "type": "CreativeWork"
      }, 
      {
        "id": "sg:pub.10.1038/381120b0", 
        "sameAs": [
          "https://app.dimensions.ai/details/publication/pub.1023527169", 
          "https://doi.org/10.1038/381120b0"
        ], 
        "type": "CreativeWork"
      }, 
      {
        "id": "sg:pub.10.1038/s41598-016-0001-8", 
        "sameAs": [
          "https://app.dimensions.ai/details/publication/pub.1085379182", 
          "https://doi.org/10.1038/s41598-016-0001-8"
        ], 
        "type": "CreativeWork"
      }, 
      {
        "id": "sg:pub.10.1038/35107092", 
        "sameAs": [
          "https://app.dimensions.ai/details/publication/pub.1051857260", 
          "https://doi.org/10.1038/35107092"
        ], 
        "type": "CreativeWork"
      }, 
      {
        "id": "sg:pub.10.1038/s41564-019-0645-9", 
        "sameAs": [
          "https://app.dimensions.ai/details/publication/pub.1124190552", 
          "https://doi.org/10.1038/s41564-019-0645-9"
        ], 
        "type": "CreativeWork"
      }, 
      {
        "id": "sg:pub.10.1038/ng.1038", 
        "sameAs": [
          "https://app.dimensions.ai/details/publication/pub.1030251531", 
          "https://doi.org/10.1038/ng.1038"
        ], 
        "type": "CreativeWork"
      }
    ], 
    "datePublished": "2022-01-10", 
    "datePublishedReg": "2022-01-10", 
    "description": "Antibiotic-resistance genes (ARGs) regulated by invertible promoters can mitigate the fitness cost of maintaining ARGs in the absence of antibiotics and could potentially prolong the persistence of ARGs in bacterial populations. However, the origin, prevalence, and distribution of these ARGs regulated by invertible promoters remains poorly understood. Here, we sought to assess the threat posed by ARGs regulated by invertible promoters by systematically searching for ARGs regulated by invertible promoters in the human gut microbiome and examining their origin, prevalence, and distribution. Through metagenomic assembly of 2227 human gut metagenomes and genomic analysis of the Unified Human Gastrointestinal Genome (UHGG) collection, we identified ARGs regulated by invertible promoters and categorized them into three classes based on the invertase-regulating phase variation. In the human gut microbiome, ARGs regulated by invertible promoters are exclusively found in Bacteroidales species. Through genomic analysis, we observed that ARGs regulated by invertible promoters have convergently originated from ARG insertions into glycan-synthesis loci that were regulated by invertible promoters at least three times. Moreover, all three classes of invertible promoters regulating ARGs are located within integrative conjugative elements (ICEs). Therefore, horizontal transfer via ICEs could explain the wide taxonomic distribution of ARGs regulated by invertible promoters. Overall, these findings reveal that glycan-synthesis loci regulated by invertible promoters in Bacteroidales species are an important hotspot for the emergence of clinically-relevant ARGs regulated by invertible promoters.", 
    "genre": "article", 
    "id": "sg:pub.10.1038/s41522-021-00260-1", 
    "inLanguage": "en", 
    "isAccessibleForFree": true, 
    "isPartOf": [
      {
        "id": "sg:journal.1052387", 
        "issn": [
          "2055-5008"
        ], 
        "name": "npj Biofilms and Microbiomes", 
        "publisher": "Springer Nature", 
        "type": "Periodical"
      }, 
      {
        "issueNumber": "1", 
        "type": "PublicationIssue"
      }, 
      {
        "type": "PublicationVolume", 
        "volumeNumber": "8"
      }
    ], 
    "keywords": [
      "antibiotic resistance genes", 
      "integrative conjugative elements", 
      "invertible promoters", 
      "genomic analysis", 
      "Unified Human Gastrointestinal Genome (UHGG) collection", 
      "wide taxonomic distribution", 
      "persistence of ARGs", 
      "human gut", 
      "human gut metagenomes", 
      "human gut microbiome", 
      "taxonomic distribution", 
      "Bacteroidales species", 
      "fitness costs", 
      "gut metagenomes", 
      "horizontal transfer", 
      "important hotspot", 
      "absence of antibiotics", 
      "genome collection", 
      "relevant antibiotic resistance genes", 
      "metagenomic assembly", 
      "bacterial populations", 
      "resistance genes", 
      "promoter", 
      "conjugative elements", 
      "genes", 
      "loci", 
      "Bacteroidales", 
      "gut microbiome", 
      "metagenomes", 
      "gut", 
      "phase variation", 
      "species", 
      "microbiome", 
      "assembly", 
      "origin", 
      "hotspots", 
      "persistence", 
      "insertion", 
      "population", 
      "distribution", 
      "absence", 
      "variation", 
      "analysis", 
      "threat", 
      "emergence", 
      "class", 
      "antibiotics", 
      "reservoir", 
      "collection", 
      "elements", 
      "transfer", 
      "findings", 
      "time", 
      "prevalence", 
      "cost"
    ], 
    "name": "Bacteroidales species in the human gut are a reservoir of antibiotic resistance genes regulated by invertible promoters", 
    "pagination": "1", 
    "productId": [
      {
        "name": "dimensions_id", 
        "type": "PropertyValue", 
        "value": [
          "pub.1144548355"
        ]
      }, 
      {
        "name": "doi", 
        "type": "PropertyValue", 
        "value": [
          "10.1038/s41522-021-00260-1"
        ]
      }, 
      {
        "name": "pubmed_id", 
        "type": "PropertyValue", 
        "value": [
          "35013297"
        ]
      }
    ], 
    "sameAs": [
      "https://doi.org/10.1038/s41522-021-00260-1", 
      "https://app.dimensions.ai/details/publication/pub.1144548355"
    ], 
    "sdDataset": "articles", 
    "sdDatePublished": "2022-06-01T22:26", 
    "sdLicense": "https://scigraph.springernature.com/explorer/license/", 
    "sdPublisher": {
      "name": "Springer Nature - SN SciGraph project", 
      "type": "Organization"
    }, 
    "sdSource": "s3://com-springernature-scigraph/baseset/20220601/entities/gbq_results/article/article_940.jsonl", 
    "type": "ScholarlyArticle", 
    "url": "https://doi.org/10.1038/s41522-021-00260-1"
  }
]
 

Download the RDF metadata as:  json-ld nt turtle xml License info

HOW TO GET THIS DATA PROGRAMMATICALLY:

JSON-LD is a popular format for linked data which is fully compatible with JSON.

curl -H 'Accept: application/ld+json' 'https://scigraph.springernature.com/pub.10.1038/s41522-021-00260-1'

N-Triples is a line-based linked data format ideal for batch operations.

curl -H 'Accept: application/n-triples' 'https://scigraph.springernature.com/pub.10.1038/s41522-021-00260-1'

Turtle is a human-readable linked data format.

curl -H 'Accept: text/turtle' 'https://scigraph.springernature.com/pub.10.1038/s41522-021-00260-1'

RDF/XML is a standard XML format for linked data.

curl -H 'Accept: application/rdf+xml' 'https://scigraph.springernature.com/pub.10.1038/s41522-021-00260-1'


 

This table displays all metadata directly associated to this object as RDF triples.

198 TRIPLES      22 PREDICATES      97 URIs      79 LITERALS      13 BLANK NODES

Subject Predicate Object
1 sg:pub.10.1038/s41522-021-00260-1 schema:about N12f519ed77984d7dbffb2ef68db9b32f
2 N20f8dab976f84e1887d856e8e0d2b892
3 N4e5649856c7b41398cdb42428b963dcd
4 Na733c023cfe441eeb0139d3c748c8401
5 Nc09ca0b3925e4dd4b73a1ad78f04fe67
6 Nd29dc5aea7bd4522bf214c9b74540fbc
7 anzsrc-for:06
8 anzsrc-for:0604
9 schema:author Nd545a7868345456684cdc15952d676c7
10 schema:citation sg:pub.10.1007/bf00383309
11 sg:pub.10.1038/35107092
12 sg:pub.10.1038/381120b0
13 sg:pub.10.1038/ng.1038
14 sg:pub.10.1038/nmeth.1923
15 sg:pub.10.1038/nrmicro2319
16 sg:pub.10.1038/s41564-019-0645-9
17 sg:pub.10.1038/s41587-020-0603-3
18 sg:pub.10.1038/s41598-016-0001-8
19 sg:pub.10.1186/1471-2105-5-113
20 schema:datePublished 2022-01-10
21 schema:datePublishedReg 2022-01-10
22 schema:description Antibiotic-resistance genes (ARGs) regulated by invertible promoters can mitigate the fitness cost of maintaining ARGs in the absence of antibiotics and could potentially prolong the persistence of ARGs in bacterial populations. However, the origin, prevalence, and distribution of these ARGs regulated by invertible promoters remains poorly understood. Here, we sought to assess the threat posed by ARGs regulated by invertible promoters by systematically searching for ARGs regulated by invertible promoters in the human gut microbiome and examining their origin, prevalence, and distribution. Through metagenomic assembly of 2227 human gut metagenomes and genomic analysis of the Unified Human Gastrointestinal Genome (UHGG) collection, we identified ARGs regulated by invertible promoters and categorized them into three classes based on the invertase-regulating phase variation. In the human gut microbiome, ARGs regulated by invertible promoters are exclusively found in Bacteroidales species. Through genomic analysis, we observed that ARGs regulated by invertible promoters have convergently originated from ARG insertions into glycan-synthesis loci that were regulated by invertible promoters at least three times. Moreover, all three classes of invertible promoters regulating ARGs are located within integrative conjugative elements (ICEs). Therefore, horizontal transfer via ICEs could explain the wide taxonomic distribution of ARGs regulated by invertible promoters. Overall, these findings reveal that glycan-synthesis loci regulated by invertible promoters in Bacteroidales species are an important hotspot for the emergence of clinically-relevant ARGs regulated by invertible promoters.
23 schema:genre article
24 schema:inLanguage en
25 schema:isAccessibleForFree true
26 schema:isPartOf N238ba67fd10f4f378e98eb334fd2d3f1
27 N5755c1369f424405bc2e3bfc5ce7450e
28 sg:journal.1052387
29 schema:keywords Bacteroidales
30 Bacteroidales species
31 Unified Human Gastrointestinal Genome (UHGG) collection
32 absence
33 absence of antibiotics
34 analysis
35 antibiotic resistance genes
36 antibiotics
37 assembly
38 bacterial populations
39 class
40 collection
41 conjugative elements
42 cost
43 distribution
44 elements
45 emergence
46 findings
47 fitness costs
48 genes
49 genome collection
50 genomic analysis
51 gut
52 gut metagenomes
53 gut microbiome
54 horizontal transfer
55 hotspots
56 human gut
57 human gut metagenomes
58 human gut microbiome
59 important hotspot
60 insertion
61 integrative conjugative elements
62 invertible promoters
63 loci
64 metagenomes
65 metagenomic assembly
66 microbiome
67 origin
68 persistence
69 persistence of ARGs
70 phase variation
71 population
72 prevalence
73 promoter
74 relevant antibiotic resistance genes
75 reservoir
76 resistance genes
77 species
78 taxonomic distribution
79 threat
80 time
81 transfer
82 variation
83 wide taxonomic distribution
84 schema:name Bacteroidales species in the human gut are a reservoir of antibiotic resistance genes regulated by invertible promoters
85 schema:pagination 1
86 schema:productId N32461c0ffb1844b280ea10ab5565d169
87 N6975f1bc8c01487aaa7f174e1de7df0a
88 N70553c7e913d419ba0fc9ce85b94acc2
89 schema:sameAs https://app.dimensions.ai/details/publication/pub.1144548355
90 https://doi.org/10.1038/s41522-021-00260-1
91 schema:sdDatePublished 2022-06-01T22:26
92 schema:sdLicense https://scigraph.springernature.com/explorer/license/
93 schema:sdPublisher N5d655784306e47989f66a40505267e93
94 schema:url https://doi.org/10.1038/s41522-021-00260-1
95 sgo:license sg:explorer/license/
96 sgo:sdDataset articles
97 rdf:type schema:ScholarlyArticle
98 N12f519ed77984d7dbffb2ef68db9b32f schema:inDefinedTermSet https://www.nlm.nih.gov/mesh/
99 schema:name Metagenomics
100 rdf:type schema:DefinedTerm
101 N20f8dab976f84e1887d856e8e0d2b892 schema:inDefinedTermSet https://www.nlm.nih.gov/mesh/
102 schema:name Drug Resistance, Microbial
103 rdf:type schema:DefinedTerm
104 N238ba67fd10f4f378e98eb334fd2d3f1 schema:volumeNumber 8
105 rdf:type schema:PublicationVolume
106 N32461c0ffb1844b280ea10ab5565d169 schema:name dimensions_id
107 schema:value pub.1144548355
108 rdf:type schema:PropertyValue
109 N4e5649856c7b41398cdb42428b963dcd schema:inDefinedTermSet https://www.nlm.nih.gov/mesh/
110 schema:name Phase Variation
111 rdf:type schema:DefinedTerm
112 N5755c1369f424405bc2e3bfc5ce7450e schema:issueNumber 1
113 rdf:type schema:PublicationIssue
114 N5d655784306e47989f66a40505267e93 schema:name Springer Nature - SN SciGraph project
115 rdf:type schema:Organization
116 N6975f1bc8c01487aaa7f174e1de7df0a schema:name doi
117 schema:value 10.1038/s41522-021-00260-1
118 rdf:type schema:PropertyValue
119 N70553c7e913d419ba0fc9ce85b94acc2 schema:name pubmed_id
120 schema:value 35013297
121 rdf:type schema:PropertyValue
122 N96c6015342d24fbb97e8fbf8268fd268 rdf:first sg:person.01024545742.89
123 rdf:rest Nfb4e9a3cb6c34bc9a5ca5a9036b64669
124 Na733c023cfe441eeb0139d3c748c8401 schema:inDefinedTermSet https://www.nlm.nih.gov/mesh/
125 schema:name Humans
126 rdf:type schema:DefinedTerm
127 Nc09ca0b3925e4dd4b73a1ad78f04fe67 schema:inDefinedTermSet https://www.nlm.nih.gov/mesh/
128 schema:name Anti-Bacterial Agents
129 rdf:type schema:DefinedTerm
130 Nd29dc5aea7bd4522bf214c9b74540fbc schema:inDefinedTermSet https://www.nlm.nih.gov/mesh/
131 schema:name Gastrointestinal Microbiome
132 rdf:type schema:DefinedTerm
133 Nd545a7868345456684cdc15952d676c7 rdf:first sg:person.012071475727.80
134 rdf:rest N96c6015342d24fbb97e8fbf8268fd268
135 Nfb4e9a3cb6c34bc9a5ca5a9036b64669 rdf:first sg:person.01227353652.96
136 rdf:rest rdf:nil
137 anzsrc-for:06 schema:inDefinedTermSet anzsrc-for:
138 schema:name Biological Sciences
139 rdf:type schema:DefinedTerm
140 anzsrc-for:0604 schema:inDefinedTermSet anzsrc-for:
141 schema:name Genetics
142 rdf:type schema:DefinedTerm
143 sg:journal.1052387 schema:issn 2055-5008
144 schema:name npj Biofilms and Microbiomes
145 schema:publisher Springer Nature
146 rdf:type schema:Periodical
147 sg:person.01024545742.89 schema:affiliation grid-institutes:grid.164295.d
148 schema:familyName Hall
149 schema:givenName A. Brantley
150 schema:sameAs https://app.dimensions.ai/discover/publication?and_facet_researcher=ur.01024545742.89
151 rdf:type schema:Person
152 sg:person.012071475727.80 schema:affiliation grid-institutes:grid.280285.5
153 schema:familyName Yan
154 schema:givenName Wei
155 schema:sameAs https://app.dimensions.ai/discover/publication?and_facet_researcher=ur.012071475727.80
156 rdf:type schema:Person
157 sg:person.01227353652.96 schema:affiliation grid-institutes:grid.280285.5
158 schema:familyName Jiang
159 schema:givenName Xiaofang
160 schema:sameAs https://app.dimensions.ai/discover/publication?and_facet_researcher=ur.01227353652.96
161 rdf:type schema:Person
162 sg:pub.10.1007/bf00383309 schema:sameAs https://app.dimensions.ai/details/publication/pub.1016899890
163 https://doi.org/10.1007/bf00383309
164 rdf:type schema:CreativeWork
165 sg:pub.10.1038/35107092 schema:sameAs https://app.dimensions.ai/details/publication/pub.1051857260
166 https://doi.org/10.1038/35107092
167 rdf:type schema:CreativeWork
168 sg:pub.10.1038/381120b0 schema:sameAs https://app.dimensions.ai/details/publication/pub.1023527169
169 https://doi.org/10.1038/381120b0
170 rdf:type schema:CreativeWork
171 sg:pub.10.1038/ng.1038 schema:sameAs https://app.dimensions.ai/details/publication/pub.1030251531
172 https://doi.org/10.1038/ng.1038
173 rdf:type schema:CreativeWork
174 sg:pub.10.1038/nmeth.1923 schema:sameAs https://app.dimensions.ai/details/publication/pub.1006541515
175 https://doi.org/10.1038/nmeth.1923
176 rdf:type schema:CreativeWork
177 sg:pub.10.1038/nrmicro2319 schema:sameAs https://app.dimensions.ai/details/publication/pub.1000198743
178 https://doi.org/10.1038/nrmicro2319
179 rdf:type schema:CreativeWork
180 sg:pub.10.1038/s41564-019-0645-9 schema:sameAs https://app.dimensions.ai/details/publication/pub.1124190552
181 https://doi.org/10.1038/s41564-019-0645-9
182 rdf:type schema:CreativeWork
183 sg:pub.10.1038/s41587-020-0603-3 schema:sameAs https://app.dimensions.ai/details/publication/pub.1129483269
184 https://doi.org/10.1038/s41587-020-0603-3
185 rdf:type schema:CreativeWork
186 sg:pub.10.1038/s41598-016-0001-8 schema:sameAs https://app.dimensions.ai/details/publication/pub.1085379182
187 https://doi.org/10.1038/s41598-016-0001-8
188 rdf:type schema:CreativeWork
189 sg:pub.10.1186/1471-2105-5-113 schema:sameAs https://app.dimensions.ai/details/publication/pub.1040413794
190 https://doi.org/10.1186/1471-2105-5-113
191 rdf:type schema:CreativeWork
192 grid-institutes:grid.164295.d schema:alternateName Center for Bioinformatics and Computational Biology, University of Maryland, College Park, Maryland, USA
193 schema:name Center for Bioinformatics and Computational Biology, University of Maryland, College Park, Maryland, USA
194 Department of Cell Biology and Molecular Genetics, University of Maryland, College Park, Maryland, USA
195 rdf:type schema:Organization
196 grid-institutes:grid.280285.5 schema:alternateName National Library of Medicine, National Institutes of Health, Bethesda, Maryland, USA
197 schema:name National Library of Medicine, National Institutes of Health, Bethesda, Maryland, USA
198 rdf:type schema:Organization
 




Preview window. Press ESC to close (or click here)


...