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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="CD6F3526FFCA2529477EFC45FB7024F9" 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. KINNARIDIS 2021, SUBSP. NOV." docType="treatment" docVersion="7" lastPageNumber="18" 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="18" 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:roleTerm>Author</mods:roleTerm>
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<mods:namePart>Zheng, Jinshui</mods:namePart>
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<mods:roleTerm>Author</mods:roleTerm>
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<mods:namePart>Liu, Junhong</mods:namePart>
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<mods:roleTerm>Author</mods:roleTerm>
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<mods:namePart>Quevedo, Rodrigo Margain</mods:namePart>
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<mods:roleTerm>Author</mods:roleTerm>
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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:roleTerm>Author</mods:roleTerm>
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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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<treatment ID-DOI="http://doi.org/10.5281/zenodo.6310185" ID-GBIF-Taxon="193366147" ID-Zenodo-Dep="6310185" LSID="urn:lsid:plazi:treatment:CD6F3526FFCA2529477EFC45FB7024F9" httpUri="http://treatment.plazi.org/id/CD6F3526FFCA2529477EFC45FB7024F9" lastPageNumber="18" pageId="17" pageNumber="18">
<subSubSection pageId="17" pageNumber="18" type="nomenclature">
<paragraph blockId="17.[120,766,918,1956]" pageId="17" pageNumber="18">
<heading allCaps="true" bold="true" fontSize="12" level="2" pageId="17" pageNumber="18" reason="3">
<emphasis bold="true" pageId="17" pageNumber="18">
DESCRIPTION OF
<taxonomicName authority="SUBSP. KINNARIDIS" authorityName="SUBSP. KINNARIDIS" authorityYear="2021" class="Bacilli" family="Lactobacillaceae" genus="Limosilactobacillus" higherTaxonomySource="GBIF" kingdom="Bacteria" order="Lactobacillales" pageId="17" pageNumber="18" phylum="Firmicutes" rank="species" species="reuteri" status="SUBSP. NOV.">
<emphasis bold="true" italics="true" pageId="17" pageNumber="18">LIMOSILACTOBACILLUS REUTERI</emphasis>
SUBSP.
<emphasis bold="true" box="[360,526,955,984]" italics="true" pageId="17" pageNumber="18">KINNARIDIS</emphasis>
</taxonomicName>
<taxonomicNameLabel box="[534,710,955,984]" pageId="17" pageNumber="18" rank="subSpecies">SUBSP. NOV.</taxonomicNameLabel>
</emphasis>
</heading>
</paragraph>
</subSubSection>
<subSubSection pageId="17" pageNumber="18" type="etymology">
<paragraph blockId="17.[120,766,918,1956]" pageId="17" pageNumber="18">
<taxonomicName authorityName="Li &amp; Cheng &amp; Zheng &amp; Liu &amp; Quevedo &amp; Li &amp; Roos &amp; Gänzle &amp; Walter" authorityYear="2021" box="[121,603,997,1021]" class="Bacilli" family="Lactobacillaceae" genus="Limosilactobacillus" higherTaxonomySource="GBIF" kingdom="Bacteria" order="Lactobacillales" pageId="17" pageNumber="18" phylum="Firmicutes" rank="subSpecies" species="reuteri" subSpecies="kinnaridis">
<emphasis box="[121,406,997,1021]" italics="true" pageId="17" pageNumber="18">Limosilactobacillus reuteri</emphasis>
subsp.
<emphasis box="[495,603,997,1021]" italics="true" pageId="17" pageNumber="18">kinnaridis</emphasis>
</taxonomicName>
(kin.na ri.dis. N.L. 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="[243,349,1028,1052]" pageId="17" pageNumber="18" rank="subSpecies" status="SUBSP. NOV." subSpecies="Kinnaridis">
<emphasis box="[243,349,1028,1052]" italics="true" pageId="17" pageNumber="18">kinnaridis</emphasis>
</taxonomicName>
of Kinnaris, referring to kinnaris, halfbird, half-woman creatures of South-East Asian mythology and reflecting occurrence of strains of this subspecies in birds and in humans. The name also reflects the use of this subspecies in probiotics, as according to south-east Asian mythology, Kinnaris are believed to come from the Himalayas and watch over the well-being of humans in times of trouble or danger).
</paragraph>
</subSubSection>
<subSubSection pageId="17" pageNumber="18" type="description">
<paragraph blockId="17.[120,766,918,1956]" lastBlockId="17.[828,1467,183,716]" pageId="17" pageNumber="18">
<taxonomicName authorityName="SUBSP. KINNARIDIS" authorityYear="2021" box="[121,222,1258,1281]" class="Bacilli" family="Lactobacillaceae" genus="Limosilactobacillus" higherTaxonomySource="GBIF" kingdom="Bacteria" order="Lactobacillales" pageId="17" pageNumber="18" phylum="Firmicutes" rank="species" species="reuteri">
<emphasis box="[121,222,1258,1281]" italics="true" pageId="17" pageNumber="18">L. reuteri</emphasis>
</taxonomicName>
strains clustered in lineage VI (
<figureCitation box="[577,639,1257,1281]" 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="17" pageNumber="18">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="[122,428,1288,1312]" class="Bacilli" family="Lactobacillaceae" genus="Limosilactobacillus" higherTaxonomySource="GBIF" kingdom="Bacteria" order="Lactobacillales" pageId="17" pageNumber="18" phylum="Firmicutes" rank="subSpecies" species="reuteri" subSpecies="kinnaridis">
<emphasis box="[122,226,1289,1312]" italics="true" pageId="17" pageNumber="18">L. reuteri</emphasis>
subsp.
<emphasis box="[316,428,1288,1312]" italics="true" pageId="17" pageNumber="18">kinnaridis</emphasis>
</taxonomicName>
and they were isolated from poultry and humans [
<bibRefCitation author="Duar RM &amp; Frese SA &amp; Lin XB &amp; Fernando SC &amp; Burkey TE" box="[361,377,1319,1343]" pageId="17" pageNumber="18" 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="[390,406,1319,1342]" pageId="17" pageNumber="18" 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 98.2100.0% with each other and ANI values of 93.896.6 % with other
<taxonomicName authorityName="SUBSP. KINNARIDIS" authorityYear="2021" box="[420,523,1381,1404]" class="Bacilli" family="Lactobacillaceae" genus="Limosilactobacillus" higherTaxonomySource="GBIF" kingdom="Bacteria" order="Lactobacillales" pageId="17" pageNumber="18" phylum="Firmicutes" rank="species" species="reuteri">
<emphasis box="[420,523,1381,1404]" italics="true" pageId="17" pageNumber="18">L. reuteri</emphasis>
</taxonomicName>
strains belonging to different subspecies (
<figureCitation box="[376,447,1411,1435]" 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="17" pageNumber="18">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, methylα- D-glucopyranoside and turanose is strain-specific; acid is not produced from D-xylose, D-fructose, D-mannose, aesculin, glycerol, erythritol, D-arabinose,L-xylose,D-adonitol, methyl
<emphasis box="[711,724,1595,1619]" italics="true" pageId="17" pageNumber="18">β</emphasis>
-Dxylopyranoside, L-sorbose,L-rhamnose, dulcitol, inositol, D-mannitol, D-sorbitol, methyl α- D-mannopyranoside,
<emphasis box="[121,140,1687,1710]" italics="true" pageId="17" pageNumber="18">N</emphasis>
-acetylglucosamine, amygdalin, arbutin, salicin, cellobiose, trehalose, inulin, melezitose, starch, glycogen, xylitol, gentiobiose, 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 (
<figureCitation box="[516,578,1840,1864]" 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="17" pageNumber="18">Fig. 3</figureCitation>
) and a previous study [
<bibRefCitation author="Duar RM &amp; Frese SA &amp; Lin XB &amp; Fernando SC &amp; Burkey TE" box="[195,211,1871,1895]" pageId="17" pageNumber="18" 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>
], AFLP and MLSA (using concatenated sequences of
<emphasis box="[155,190,1901,1925]" italics="true" pageId="17" pageNumber="18">ddl</emphasis>
,
<emphasis box="[208,243,1901,1925]" italics="true" pageId="17" pageNumber="18">pkt</emphasis>
,
<emphasis box="[261,307,1901,1925]" italics="true" pageId="17" pageNumber="18">leuS</emphasis>
,
<emphasis box="[325,376,1902,1925]" italics="true" pageId="17" pageNumber="18">gyrB</emphasis>
,
<emphasis box="[395,443,1901,1925]" italics="true" pageId="17" pageNumber="18">dltA</emphasis>
,
<emphasis box="[461,517,1902,1925]" italics="true" pageId="17" pageNumber="18">rpoA</emphasis>
and
<emphasis box="[582,632,1902,1925]" italics="true" pageId="17" pageNumber="18">recA</emphasis>
genes) [
<bibRefCitation author="Oh PL &amp; Benson AK &amp; Peterson DA &amp; Patil PB &amp; Moriyama EN" box="[735,751,1902,1925]" pageId="17" pageNumber="18" 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>
] indicate that strains clustered in this lineage are adapted to poultry and also occur in humans. Experimental test has revealed that strains of
<taxonomicName authorityName="Li &amp; Cheng &amp; Zheng &amp; Liu &amp; Quevedo &amp; Li &amp; Roos &amp; Gänzle &amp; Walter" authorityYear="2021" box="[1156,1467,214,238]" class="Bacilli" family="Lactobacillaceae" genus="Limosilactobacillus" higherTaxonomySource="GBIF" kingdom="Bacteria" order="Lactobacillales" pageId="17" pageNumber="18" phylum="Firmicutes" rank="subSpecies" species="reuteri" subSpecies="kinnaridis">
<emphasis box="[1156,1262,215,238]" italics="true" pageId="17" pageNumber="18">L. reuteri</emphasis>
subsp.
<emphasis box="[1355,1467,214,238]" italics="true" pageId="17" pageNumber="18">kinnaridis</emphasis>
</taxonomicName>
displayed elevated fitness in chickens but not in humans [
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], suggesting that this subspecies is autochthonous of chicken and share an evolutionary history with poultry. Strains of this subspecies possess the
<emphasis box="[1280,1466,342,366]" italics="true" pageId="17" pageNumber="18">pdu-cbi-cob-hem</emphasis>
cluster (
<emphasis box="[921,963,373,397]" italics="true" pageId="17" pageNumber="18">pdu</emphasis>
cluster) [
<bibRefCitation author="Frese SA &amp; Benson AK &amp; Tannock GW &amp; Loach DM &amp; Kim J" box="[1074,1090,373,397]" pageId="17" pageNumber="18" 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="[1105,1121,374,398]" pageId="17" pageNumber="18" 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>
], which equips them with the ability to utilize 1,2-propanediol and glycerol as electron acceptors [
<bibRefCitation author="Cheng CC &amp; Duar RM &amp; Lin X &amp; Perez-Munoz ME &amp; Tollenaar S" box="[946,976,437,461]" pageId="17" pageNumber="18" refId="ref16011" refString="16. Cheng CC, Duar RM, Lin X, Perez-Munoz ME, Tollenaar S et al. Ecological importance of cross-feeding of the intermediate metabolite 1,2 - propanediol between bacterial gut symbionts. Appl Environ Microbiol 2020; 86: e 00190 - 20." type="journal volume" year="2020">16</bibRefCitation>
,
<bibRefCitation author="Luthi-Peng Q &amp; Dileme FB &amp; Puhan Z." box="[988,1016,437,461]" pageId="17" pageNumber="18" pagination="289 - 296" refId="ref16896" refString="39. Luthi-Peng Q, Dileme FB, Puhan Z. Effect of glucose on glycerol bioconversion by Lactobacillus reuteri. Appl Microbiol Biotechnol 2002; 59: 289 - 296." type="journal article" year="2002">39</bibRefCitation>
,
<bibRefCitation author="Dishisha T &amp; Pereyra LP &amp; Pyo SH &amp; Britton RA &amp; Hatti-Kaul R." box="[1028,1057,437,461]" pageId="17" pageNumber="18" pagination="76" refId="ref16928" refString="40. Dishisha T, Pereyra LP, Pyo SH, Britton RA, Hatti-Kaul R. Flux analysis of the Lactobacillus reuteri propanediol-utilization pathway for production of 3 - hydroxypropionaldehyde, 3 - hydroxypropionic acid and 1,3 - propanediol from glycerol. Microb Cell Fact 2014; 13: 76." type="journal article" year="2014">40</bibRefCitation>
] and to produce the broad-spectrum antimicrobial compound reuterin [
<bibRefCitation author="Walter J &amp; Britton RA &amp; Roos S." box="[1233,1249,469,493]" pageId="17" pageNumber="18" 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>
,
<bibRefCitation author="Spinler JK &amp; Sontakke A &amp; Hollister EB &amp; Venable SF &amp; Oh PL" box="[1265,1297,469,493]" pageId="17" pageNumber="18" pagination="1772 - 1789" refId="ref16693" refString="34. Spinler JK, Sontakke A, Hollister EB, Venable SF, Oh PL, et al. From prediction to function using evolutionary genomics: humanspecific ecotypes of Lactobacillus reuteri have diverse probiotic functions. Genome Biol Evol 2014; 6: 1772 - 1789." type="journal article" year="2014">34</bibRefCitation>
]. These strains are immunostimulatory; specifically, they stimulate the production of IL-7, IL-12 and IL-13, but suppress the production of IL-5 [
<bibRefCitation author="Spinler JK &amp; Sontakke A &amp; Hollister EB &amp; Venable SF &amp; Oh PL" box="[1052,1085,565,589]" pageId="17" pageNumber="18" pagination="1772 - 1789" refId="ref16693" refString="34. Spinler JK, Sontakke A, Hollister EB, Venable SF, Oh PL, et al. From prediction to function using evolutionary genomics: humanspecific ecotypes of Lactobacillus reuteri have diverse probiotic functions. Genome Biol Evol 2014; 6: 1772 - 1789." type="journal article" year="2014">34</bibRefCitation>
]. In addition, strains belonging to this subspecies synthesize folate
<emphasis box="[1208,1296,596,620]" italics="true" pageId="17" pageNumber="18">de novo</emphasis>
[
<bibRefCitation author="Spinler JK &amp; Sontakke A &amp; Hollister EB &amp; Venable SF &amp; Oh PL" box="[1312,1345,596,620]" pageId="17" pageNumber="18" pagination="1772 - 1789" refId="ref16693" refString="34. Spinler JK, Sontakke A, Hollister EB, Venable SF, Oh PL, et al. From prediction to function using evolutionary genomics: humanspecific ecotypes of Lactobacillus reuteri have diverse probiotic functions. Genome Biol Evol 2014; 6: 1772 - 1789." type="journal article" year="2014">34</bibRefCitation>
].
</paragraph>
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The
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strain, AP3
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(=DSM 110703
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=
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), was isolated from the gastrointestinal tract of an Argus Pheasant, with a DNA G+C content of 38.6mol%.
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