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<document ID-DOI="10.1099/ijsem.0.004644" ID-GBIF-Dataset="6b321035-fd9c-4b25-a3b6-79a05a309793" ID-ISSN="1466-5034" ID-PMC="PMC8346765" ID-PubMed="33533708" ID-Zenodo-Dep="6048739" checkinTime="1644597549702" checkinUser="felipe" docAuthor="Li, Fuyong, Cheng, Christopher C., Zheng, Jinshui, Liu, Junhong, Quevedo, Rodrigo Margain, Li, Junjie, Roos, Stefan, Gänzle, Michael G. &amp; Walter, Jens" docDate="2021" docId="CD6F3526FFC9252B443BFC00FE32248B" docLanguage="en" docName="IntJSystEvolMicrobiol.71.2.004644.pdf" docOrigin="International Journal of Systematic and Evolutionary Microbiology (004644) 71 (2)" docSource="http://dx.doi.org/10.1099/ijsem.0.004644" docStyle="DocumentStyle:C64F0A4F4C66F6FC2AD4ED89351C6242.1:IntJSystEvolMicrobiol.2017-.journal_article" docStyleId="C64F0A4F4C66F6FC2AD4ED89351C6242" docStyleName="IntJSystEvolMicrobiol.2017-.journal_article" docStyleVersion="1" docTitle="Limosilactobacillus reuteri SUBSP. RODENTIUM 2021, SUBSP. NOV." docType="treatment" docVersion="7" lastPageNumber="20" masterDocId="31564D5EFFDB25384707FFD3FFC62635" masterDocTitle="Limosilactobacillus balticus sp. nov., Limosilactobacillus agrestis sp. nov., Limosilactobacillus albertensis sp. nov., Limosilactobacillus rudii sp. nov. and Limosilactobacillus fastidiosus sp. nov., five novel Limosilactobacillus species isolated from the vertebrate gastrointestinal tract, and proposal of six subspecies of Limosilactobacillus reuteri adapted to the gastrointestinal tract of specific vertebrate hosts" masterLastPageNumber="21" masterPageNumber="1" pageNumber="19" updateTime="1668130802247" updateUser="ExternalLinkService">
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<mods:title>Limosilactobacillus balticus sp. nov., Limosilactobacillus agrestis sp. nov., Limosilactobacillus albertensis sp. nov., Limosilactobacillus rudii sp. nov. and Limosilactobacillus fastidiosus sp. nov., five novel Limosilactobacillus species isolated from the vertebrate gastrointestinal tract, and proposal of six subspecies of Limosilactobacillus reuteri adapted to the gastrointestinal tract of specific vertebrate hosts</mods:title>
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<mods:namePart>Li, Fuyong</mods:namePart>
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<mods:namePart>Cheng, Christopher C.</mods:namePart>
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<mods:namePart>Zheng, Jinshui</mods:namePart>
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<mods:namePart>Liu, Junhong</mods:namePart>
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<mods:namePart>Quevedo, Rodrigo Margain</mods:namePart>
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<mods:namePart>Li, Junjie</mods:namePart>
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<mods:namePart>Roos, Stefan</mods:namePart>
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<mods:namePart>Gänzle, Michael G.</mods:namePart>
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<mods:namePart>Walter, Jens</mods:namePart>
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DESCRIPTION OF
<taxonomicName authority="SUBSP. RODENTIUM" authorityName="SUBSP. RODENTIUM" authorityYear="2021" class="Bacilli" family="Lactobacillaceae" genus="Limosilactobacillus" higherTaxonomySource="GBIF" kingdom="Bacteria" order="Lactobacillales" pageId="18" pageNumber="19" phylum="Firmicutes" rank="species" species="reuteri" status="SUBSP. NOV.">
<emphasis bold="true" italics="true" pageId="18" pageNumber="19">LIMOSILACTOBACILLUS REUTERI</emphasis>
SUBSP.
<emphasis bold="true" box="[1067,1234,1016,1045]" italics="true" pageId="18" pageNumber="19">RODENTIUM</emphasis>
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<taxonomicNameLabel box="[1242,1418,1016,1045]" pageId="18" pageNumber="19" rank="subSpecies">SUBSP. NOV.</taxonomicNameLabel>
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<paragraph blockId="18.[827,1473,979,1956]" pageId="18" pageNumber="19">
<taxonomicName authorityName="Li &amp; Cheng &amp; Zheng &amp; Liu &amp; Quevedo &amp; Li &amp; Roos &amp; Gänzle &amp; Walter" authorityYear="2021" box="[828,1288,1058,1082]" class="Bacilli" family="Lactobacillaceae" genus="Limosilactobacillus" higherTaxonomySource="GBIF" kingdom="Bacteria" order="Lactobacillales" pageId="18" pageNumber="19" phylum="Firmicutes" rank="subSpecies" species="reuteri" subSpecies="rodentium">
<emphasis box="[828,1102,1058,1082]" italics="true" pageId="18" pageNumber="19">Limosilactobacillus reuteri</emphasis>
subsp.
<emphasis box="[1179,1288,1058,1082]" italics="true" pageId="18" pageNumber="19">rodentium</emphasis>
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(ro.den ti.um. L. pl. gen. n.
<taxonomicName authority="Li &amp; Cheng &amp; Zheng &amp; Liu &amp; Quevedo &amp; Li &amp; Roos &amp; Gänzle &amp; Walter, 2021" authorityName="Li &amp; Cheng &amp; Zheng &amp; Liu &amp; Quevedo &amp; Li &amp; Roos &amp; Gänzle &amp; Walter" authorityYear="2021" box="[940,1049,1089,1113]" pageId="18" pageNumber="19" rank="subSpecies" status="SUBSP. NOV." subSpecies="Rodentium">
<emphasis box="[940,1049,1089,1113]" italics="true" pageId="18" pageNumber="19">rodentium</emphasis>
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of gnawing animals, reflecting adaptation of the subspecies to rodents).
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<taxonomicName authorityName="SUBSP. RODENTIUM" authorityYear="2021" box="[828,928,1166,1189]" class="Bacilli" family="Lactobacillaceae" genus="Limosilactobacillus" higherTaxonomySource="GBIF" kingdom="Bacteria" order="Lactobacillales" pageId="18" pageNumber="19" phylum="Firmicutes" rank="species" species="reuteri">
<emphasis box="[828,928,1166,1189]" italics="true" pageId="18" pageNumber="19">L. reuteri</emphasis>
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strains clustered in lineage III (
<figureCitation box="[1284,1346,1165,1189]" captionStart="Fig" captionStartId="11.[185,216,1007,1026]" captionTargetBox="[227,1361,181,954]" captionTargetId="figure-462@11.[227,1361,181,954]" captionTargetPageId="11" captionText="Fig. 3. A maximum-likelihood phylogenetic tree reconstructed using core genes (n=100) identified from whole-genome sequences, showing the evolutionary relationships among six L. reuteri subspecies.The tree was reconstructed using 33 L. reuteri genomes available in public databases (n=6 for L. reuteri subsp. kinnaridis, n=2 for L. reuteri subsp. porcinus, n=5 for L. reuteri subsp. murium, n=10 for L. reuteri subsp. reuteri, n=5 for L. reuteri subsp. suis and n=5 for L. reuteri subsp. rodentium) and L. balticus BG-AF3-AT was used as an outgroup. Further information on the involved genome sequences is listed in Table S1. The tree was inferred based on the GTR+G model with 1000 bootstrap replicates and only bootstrap values above 60% are shown. The tree was drawn with iTOL [54]." figureDoi="http://doi.org/10.5281/zenodo.6048749" httpUri="https://zenodo.org/record/6048749/files/figure.png" pageId="18" pageNumber="19">Fig. 3</figureCitation>
) belong to
<taxonomicName authorityName="Li &amp; Cheng &amp; Zheng &amp; Liu &amp; Quevedo &amp; Li &amp; Roos &amp; Gänzle &amp; Walter" authorityYear="2021" box="[828,1123,1196,1220]" class="Bacilli" family="Lactobacillaceae" genus="Limosilactobacillus" higherTaxonomySource="GBIF" kingdom="Bacteria" order="Lactobacillales" pageId="18" pageNumber="19" phylum="Firmicutes" rank="subSpecies" species="reuteri" subSpecies="rodentium">
<emphasis box="[828,928,1197,1220]" italics="true" pageId="18" pageNumber="19">L. reuteri</emphasis>
subsp.
<emphasis box="[1011,1123,1196,1220]" italics="true" pageId="18" pageNumber="19">rodentium</emphasis>
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and were mainly isolated from rodents [
<bibRefCitation author="Duar RM &amp; Frese SA &amp; Lin XB &amp; Fernando SC &amp; Burkey TE" box="[924,938,1227,1251]" pageId="18" pageNumber="19" refId="ref15514" refString="5. Duar RM, Frese SA, Lin XB, Fernando SC, Burkey TE et al. Experimental evaluation of host adaptation of Lactobacillus reuteri to different vertebrate species. Appl Environ Microbiol 2017; 83: e 00132 - 17." type="journal volume" year="2017">5</bibRefCitation>
<bibRefCitation author="Oh PL &amp; Benson AK &amp; Peterson DA &amp; Patil PB &amp; Moriyama EN" box="[956,971,1227,1251]" pageId="18" pageNumber="19" pagination="377 - 387" refId="ref15599" refString="7. Oh PL, Benson AK, Peterson DA, Patil PB, Moriyama EN et al. Diversification of the gut symbiont Lactobacillus reuteri as a result of host-driven evolution. Isme J 2010; 4: 377 - 387." type="journal article" year="2010">7</bibRefCitation>
]. Strains of this subspecies have ANI values of 96.198.9 % with each other and ANI values of 93.896.3% with other
<taxonomicName authorityName="SUBSP. RODENTIUM" authorityYear="2021" box="[949,1049,1289,1312]" class="Bacilli" family="Lactobacillaceae" genus="Limosilactobacillus" higherTaxonomySource="GBIF" kingdom="Bacteria" order="Lactobacillales" pageId="18" pageNumber="19" phylum="Firmicutes" rank="species" species="reuteri">
<emphasis box="[949,1049,1289,1312]" italics="true" pageId="18" pageNumber="19">L. reuteri</emphasis>
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strains belonging to different subspecies (
<figureCitation box="[885,947,1319,1343]" captionStart="Fig" captionStartId="12.[121,152,788,807]" captionTargetBox="[121,760,181,735]" captionTargetId="figure-792@12.[121,760,181,735]" captionTargetPageId="12" captionText="Fig. 4. Pairwise average nucleotide identity values (ANI; %) of genome sequences belonging to the same or different L. reuteri subspecies. ANI values within the same subspecies and between different subspecies were calculated for 33 L. reuteri genomes available in public databases (n=6 for L. reuteri subsp. kinnaridis, n=2 for L. reuteri subsp. porcinus, n=5 for L. reuteri subsp.murium, n=10for L. reuteri subsp.reuteri, n=5 for L. reuteri subsp. suis and n=5 for L. reuteri subsp. rodentium). Further information on the involved genome sequences is listed in Table S1." figureDoi="http://doi.org/10.5281/zenodo.6048753" httpUri="https://zenodo.org/record/6048753/files/figure.png" pageId="18" pageNumber="19">Fig. 4</figureCitation>
). Acid is produced from D-ribose,D-galactose, D-glucose, maltose, lactose, melibiose, sucrose, raffinose and potassium gluconate; acid production from L-arabinose and D-xylose is strain-specific; acid is not produced from D-fructose, D-mannose, methyl α- D-glucopyranoside, aesculin, glycerol, erythritol, D-arabinose, L-xylose, D-adonitol, methyl
<emphasis box="[1092,1106,1503,1527]" italics="true" pageId="18" pageNumber="19">β</emphasis>
-D-xylopyranoside, L-sorbose, L-rhamnose, dulcitol, inositol, D-mannitol, D-sorbitol, methyl α- D-mannopyranoside,
<emphasis box="[1224,1243,1565,1588]" italics="true" pageId="18" pageNumber="19">N</emphasis>
-acetylglucosamine, amygdalin, arbutin, salicin, cellobiose, trehalose, inulin, melezitose, starch, glycogen, xylitol, gentiobiose, turanose, D-lyxose,D-tagatose,D-fucose,L-fucose,D-arabitol, L-arabitol, potassium 2-ketogluconate or potassium 5-ketogluconate. Phylogenetic analyses based on the core genes identified in this study (
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) and a previous study [
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], AFLP and MLSA (using concatenated sequences of
<emphasis box="[1427,1461,1779,1803]" italics="true" pageId="18" pageNumber="19">ddl</emphasis>
,
<emphasis box="[828,862,1809,1833]" italics="true" pageId="18" pageNumber="19">pkt</emphasis>
,
<emphasis box="[874,919,1809,1833]" italics="true" pageId="18" pageNumber="19">leuS</emphasis>
,
<emphasis box="[932,982,1810,1833]" italics="true" pageId="18" pageNumber="19">gyrB</emphasis>
,
<emphasis box="[994,1041,1809,1833]" italics="true" pageId="18" pageNumber="19">dltA</emphasis>
,
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and
<emphasis box="[1161,1210,1810,1833]" italics="true" pageId="18" pageNumber="19">recA</emphasis>
genes) [
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] indicate that strains clustered in this lineage including the sourdough isolates are rodent-specific. Strains of
<taxonomicName authorityName="Li &amp; Cheng &amp; Zheng &amp; Liu &amp; Quevedo &amp; Li &amp; Roos &amp; Gänzle &amp; Walter" authorityYear="2021" class="Bacilli" family="Lactobacillaceae" genus="Limosilactobacillus" higherTaxonomySource="GBIF" kingdom="Bacteria" order="Lactobacillales" pageId="18" pageNumber="19" phylum="Firmicutes" rank="subSpecies" species="reuteri" subSpecies="rodentium">
<emphasis box="[1278,1384,1871,1894]" italics="true" pageId="18" pageNumber="19">L. reuteri</emphasis>
subsp.
<emphasis box="[828,941,1901,1925]" italics="true" pageId="18" pageNumber="19">rodentium</emphasis>
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displayed elevated fitness in mice through the colonization and biofilm formation on the forestomach epithelium [
<bibRefCitation author="Duar RM &amp; Frese SA &amp; Lin XB &amp; Fernando SC &amp; Burkey TE" box="[258,274,182,206]" pageId="19" pageNumber="20" refId="ref15514" refString="5. Duar RM, Frese SA, Lin XB, Fernando SC, Burkey TE et al. Experimental evaluation of host adaptation of Lactobacillus reuteri to different vertebrate species. Appl Environ Microbiol 2017; 83: e 00132 - 17." type="journal volume" year="2017">5</bibRefCitation>
,
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,
<bibRefCitation author="Frese SA &amp; Mackenzie DA &amp; Peterson DA &amp; Schmaltz R &amp; Fangman T" box="[317,346,183,207]" pageId="19" pageNumber="20" pagination="1004057" refId="ref15768" refString="11. Frese SA, Mackenzie DA, Peterson DA, Schmaltz R, Fangman T et al. Molecular characterization of host-specific biofilm formation in a vertebrate gut symbiont. PLoS Genet 2013; 9: e 1004057." type="journal article" year="2013">11</bibRefCitation>
], suggesting adaptive evolution with rodents that led to host specificity. Large surface proteins (&gt;750 aa) exist among strains belonging to this subspecies, which involve in epithelial adhesion and biofilm formation [
<bibRefCitation author="Frese SA &amp; Benson AK &amp; Tannock GW &amp; Loach DM &amp; Kim J" box="[129,146,306,330]" pageId="19" pageNumber="20" pagination="1001314" refId="ref15558" refString="6. Frese SA, Benson AK, Tannock GW, Loach DM, Kim J et al. The evolution of host specialization in the vertebrate gut symbiont Lactobacillus reuteri. PLoS Genet 2011; 7: e 1001314." type="journal article" year="2011">6</bibRefCitation>
]. A xylose operon is highly conserved for this subspecies, especially for strains originating from rodents [
<bibRefCitation author="Frese SA &amp; Benson AK &amp; Tannock GW &amp; Loach DM &amp; Kim J" box="[729,746,337,361]" pageId="19" pageNumber="20" pagination="1001314" refId="ref15558" refString="6. Frese SA, Benson AK, Tannock GW, Loach DM, Kim J et al. The evolution of host specialization in the vertebrate gut symbiont Lactobacillus reuteri. PLoS Genet 2011; 7: e 1001314." type="journal article" year="2011">6</bibRefCitation>
], and thus most strains of this subspecies could metabolize xylose that is an important substrate for gut bacteria [
<bibRefCitation author="Zhao X &amp; Ganzle MG" box="[716,748,399,423]" pageId="19" pageNumber="20" pagination="12 - 21" refId="ref17385" refString="51. Zhao X, Ganzle MG. Genetic and phenotypic analysis of carbohydrate metabolism and transport in Lactobacillus reuteri. Int J Food Microbiol 2018; 272: 12 - 21." type="journal article" year="2018">51</bibRefCitation>
]. In addition, strains of this subspecies produce the enzyme urease for acid resistance and rarely produce the antimicrobial compound reuterin [
<bibRefCitation author="Frese SA &amp; Benson AK &amp; Tannock GW &amp; Loach DM &amp; Kim J" box="[445,461,492,516]" pageId="19" pageNumber="20" pagination="1001314" refId="ref15558" refString="6. Frese SA, Benson AK, Tannock GW, Loach DM, Kim J et al. The evolution of host specialization in the vertebrate gut symbiont Lactobacillus reuteri. PLoS Genet 2011; 7: e 1001314." type="journal article" year="2011">6</bibRefCitation>
,
<bibRefCitation author="Walter J &amp; Britton RA &amp; Roos S." box="[475,491,493,517]" pageId="19" pageNumber="20" pagination="4645 - 4652" refId="ref15642" refString="8. Walter J, Britton RA, Roos S. Host-microbial symbiosis in the vertebrate gastrointestinal tract and the Lactobacillus reuteri paradigm. Proc Natl Acad Sci U S A 2011; 108 Suppl 1: 4645 - 4652." type="journal article" year="2011">8</bibRefCitation>
]. Sourdough isolates of this subspecies (LTH2584, TMW1.106, TMW1.112 and TMW1.656) produce reutericyclin, a unique antimicrobial tetramic acid with activity against Gram-positive bacteria [
<bibRefCitation author="Ganzle MG &amp; Vogel RF" box="[130,162,616,640]" pageId="19" pageNumber="20" pagination="31 - 45" refId="ref17418" refString="52. Ganzle MG, Vogel RF. Contribution of reutericyclin production to the stable persistence of Lactobacillus reuteri in an industrial sourdough fermentation. Int J Food Microbiol 2003; 80: 31 - 45." type="journal article" year="2003">52</bibRefCitation>
].
</paragraph>
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The
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strain, 100-23
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(=
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=CIP 109821
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), was isolated from the rat gastrointestinal tract [
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,
<bibRefCitation author="Wesney E &amp; Tannock GW" box="[665,695,647,671]" pageId="19" pageNumber="20" pagination="35 - 42" refId="ref17455" refString="53. Wesney E, Tannock GW. Association of rat, pig, and fowl biotypes of Lactobacilli with the stomach of gnotobiotic mice. Microb Ecol 1979; 5: 35 - 42." type="journal article" year="1979">53</bibRefCitation>
], with a DNA G+C content of 38.7mol%.
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