Ecological Importance of Cross-Feeding of the Intermediate Metabolite 1,2-Propanediol between Bacterial Gut Symbionts

ABSTRACT Cross-feeding based on the metabolite 1,2-propanediol has been proposed to have an important role in the establishment of trophic interactions among gut symbionts, but its ecological importance has not been empirically established. Here, we show that in vitro growth of Lactobacillus reuteri (syn. Limosilactobacillus reuteri) ATCC PTA 6475 is enhanced through 1,2-propanediol produced by Bifidobacterium breve UCC2003 and Escherichia coli MG1655 from the metabolization of fucose and rhamnose, respectively. Work with isogenic mutants showed that the trophic interaction is dependent on the pduCDE operon in L. reuteri, which encodes the ability to use 1,2-propanediol, and the l-fucose permease (fucP) gene in B. breve, which is required for 1,2-propanediol formation from fucose. Experiments in gnotobiotic mice revealed that, although the pduCDE operon bestows a fitness burden on L. reuteri ATCC PTA 6475 in the mouse digestive tract, the ecological performance of the strain was enhanced in the presence of B. breve UCC2003 and the mucus-degrading species Bifidobacterium bifidum. The use of the respective pduCDE and fucP mutants of L. reuteri and B. breve in the mouse experiments indicated that the trophic interaction was specifically based on 1,2-propanediol. Overall, our work established the ecological importance of cross-feeding relationships based on 1,2-propanediol for the fitness of a bacterial symbiont in the vertebrate gut. IMPORTANCE Through experiments in gnotobiotic mice that employed isogenic mutants of bacterial strains that produce (Bifidobacterium breve) and utilize (Lactobacillus reuteri) 1,2-propanediol, this study provides mechanistic insight into the ecological ramifications of a trophic interaction between gut symbionts. The findings improve our understanding on how cross-feeding influences the competitive fitness of L. reuteri in the vertebrate gut and revealed a putative selective force that shaped the evolution of the species. The findings are relevant since they provide a basis to design rational microbial-based strategies to modulate gut ecosystems, which could employ mixtures of bacterial strains that establish trophic interactions or a personalized approach based on the ability of a resident microbiota to provide resources for the incoming microbe.

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Genes Involved in Galactooligosaccharide Metabolism in Lactobacillus reuteri and Their Ecological Role in the Gastrointestinal Tract

Applied and Environmental Microbiology ◽

10.1128/aem.01788-19 ◽

2019 ◽

Vol 85 (22) ◽

Cited By ~ 3

Author(s):

Monchaya Rattanaprasert ◽

Jan-Peter van Pijkeren ◽

Amanda E. Ramer-Tait ◽

Maria Quintero ◽

Car Reen Kok ◽

...

Keyword(s):

Type Strain ◽

Wild Type Strain ◽

Lactobacillus Reuteri ◽

Selective Advantage ◽

Wild Type ◽

Carbohydrate Source ◽

Content Type ◽

Gnotobiotic Mice

ABSTRACT Strains of Lactobacillus reuteri are commonly used as probiotics due to their demonstrated therapeutic properties. Many strains of L. reuteri also utilize the prebiotic galactooligosaccharide (GOS), providing a basis for formulating synergistic synbiotics that could enhance growth or persistence of this organism in vivo. In this study, in-frame deletion mutants were constructed to characterize the molecular basis of GOS utilization in L. reuteri ATCC PTA-6475. Results suggested that GOS transport relies on a permease encoded by lacS, while a second unidentified protein may function as a galactoside transporter. Two β-galactosidases, encoded by lacA and lacLM, sequentially degrade GOS oligosaccharides and GOS disaccharides, respectively. Inactivation of lacL and lacM resulted in impaired growth in the presence of GOS and lactose. In vitro competition experiments between the wild-type and ΔlacS ΔlacM strains revealed that the GOS-utilizing genes conferred a selective advantage in media with GOS but not glucose. GOS also provided an advantage to the wild-type strain in experiments in gnotobiotic mice but only on a purified, no sucrose diet. Differences in cell numbers between GOS-fed mice and mice that did not receive GOS were small, suggesting that carbohydrates other than GOS were sufficient to support growth. On a complex diet, the ΔlacS ΔlacM strain was outcompeted by the wild-type strain in gnotobiotic mice, suggesting that lacL and lacM are involved in the utilization of alternative dietary carbohydrates. Indeed, the growth of the mutants was impaired in raffinose and stachyose, which are common in plants, demonstrating that α-galactosides may constitute alternate substrates of the GOS pathway. IMPORTANCE This study shows that lac genes in Lactobacillus reuteri encode hydrolases and transporters that are necessary for the metabolism of GOS, as well as α-galactoside substrates. Coculture experiments with the wild-type strain and a gos mutant clearly demonstrated that GOS utilization confers a growth advantage in medium containing GOS as the sole carbohydrate source. However, the wild-type strain also outcompeted the mutant in germfree mice, suggesting that GOS genes in L. reuteri also provide a basis for utilization of other carbohydrates, including α-galactosides, ordinarily present in the diets of humans and other animals. Collectively, our work provides information on the metabolism of L. reuteri in its natural niche in the gut and may provide a basis for the development of synbiotic strategies.

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Differential Toll-Like Receptor Recognition and Induction of Cytokine Profile by Bifidobacterium breve and Lactobacillus Strains of Probiotics

Clinical and Vaccine Immunology ◽

10.1128/cvi.00498-10 ◽

2011 ◽

Vol 18 (4) ◽

pp. 621-628 ◽

Cited By ~ 38

Author(s):

Theo S. Plantinga ◽

Wendy W. C. van Maren ◽

Jeroen van Bergenhenegouwen ◽

Marjolijn Hameetman ◽

Stefan Nierkens ◽

...

Keyword(s):

Pathogenic Bacteria ◽

Inflammatory Responses ◽

Lactobacillus Rhamnosus ◽

Dependent Manner ◽

Toll Like Receptor ◽

Bacterial Strains ◽

Lectin Receptors ◽

Content Type ◽

Bifidobacterium Breve ◽

Probiotic Strains

ABSTRACTThe use of probiotics as a food supplement has gained tremendous interest in the last few years as beneficial effects were reported in gut homeostasis and nutrient absorption but also in immunocompromised patients, supporting protection from colonization or infection with pathogenic bacteria or fungi. As a treatment approach for inflammatory bowel diseases, a suitable probiotic strain would ideally be one with a low immunogenic potential. Insight into the immunogenicities and types of T-cell responses induced by potentially probiotic strains allows a more rational selection of a particular strain. In the present study, the bacterial strainsBifidobacterium breve(NumRes 204),Lactobacillus rhamnosus(NumRes1), andLactobacillus casei(DN-114 001) were compared concerning their capacity to induce inflammatory responses in terms of cytokine production by human and mouse primary immune cells. It was demonstrated that theB. brevestrain induced lower levels of the proinflammatory cytokine gamma interferon (IFN-γ) than the testedL. rhamnosusandL. caseistrains. BothB. breveand lactobacilli induced cytokines in a Toll-like receptor 9 (TLR9)-dependent manner, while the lower inflammatory profile ofB. brevewas due to inhibitory effects of TLR2. No role for TLR4, NOD2, and C-type lectin receptors was apparent. In conclusion, TLR signaling is involved in the differentiation of inflammatory responses between probiotic strains used as food supplements.

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10 THE ROLE OF DIETARY L-SERINE IN THE REGULATION OF INTESTINAL MUCUS BARRIER DURING INFLAMMATION

Inflammatory Bowel Diseases ◽

10.1093/ibd/zaa010.110 ◽

2020 ◽

Vol 26 (Supplement_1) ◽

pp. S42-S42

Author(s):

Kohei Sugihara ◽

Nobuhiko Kamada

Keyword(s):

Amino Acids ◽

Amino Acid ◽

Gut Microbiota ◽

Control Diet ◽

Bacterial Strains ◽

Germ Free ◽

Intestinal Mucus ◽

Gnotobiotic Mice ◽

Mucus Barrier

Abstract Background Recent accumulating evidence suggests that amino acids have crucial roles in the maintenance of intestinal homeostasis. In inflammatory bowel disease (IBD), amino acid metabolism is changed in both host and the gut microbiota. Among amino acids, L-serine plays a central role in several metabolic processes that are essential for the growth and survival of both mammalian and bacterial cells. However, the role of L-serine in intestinal homeostasis and IBD remains incompletely understood. In this study, we investigated the effect of dietary L-serine on intestinal inflammation in a murine model of colitis. Methods Specific pathogen-free (SPF) mice were fed either a control diet (amino acid-based diet) or an L-serine-deficient diet (SDD). Colitis was induced by the treatment of dextran sodium sulfate (DSS). The gut microbiome was analyzed by 16S rRNA sequencing. We also evaluate the effect of dietary L-serine in germ-free mice and gnotobiotic mice that were colonized by a consortium of non-mucolytic bacterial strains or the consortium plus mucolytic bacterial strains. Results We found that the SDD exacerbated experimental colitis in SPF mice. However, the severity of colitis in SDD-fed mice was comparable to control diet-fed mice in germ-free condition, suggesting that the gut microbiota is required for exacerbation of colitis caused by the restriction of dietary L-serine. The gut microbiome analysis revealed that dietary L-serine restriction fosters the blooms of a mucus-degrading bacterium Akkermansia muciniphila and adherent-invasive Escherichia coli in the inflamed gut. Consistent with the expansion of mucolytic bacteria, SDD-fed mice showed a loss of the intestinal mucus layer. Dysfunction of the mucus barrier resulted in increased intestinal permeability, thereby leading to bacterial translocation to the intestinal mucosa, which subsequently increased the severity of colitis. The increased intestinal permeability and subsequent bacterial translocation were observed in SDD-fed gnotobiotic mice that colonized by mucolytic bacteria. In contrast, dietary L-serine restriction did not alter intestinal barrier integrity in gnotobiotic mice that colonized only by non-mucolytic bacteria. Conclusion Our results suggest that dietary L-serine regulates the integrity of the intestinal mucus barrier during inflammation by limiting the expansion of mucus degrading bacteria.

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Electroactivity of Phototrophic River Biofilms and Constitutive Cultivable Bacteria

Applied and Environmental Microbiology ◽

10.1128/aem.00500-11 ◽

2011 ◽

Vol 77 (15) ◽

pp. 5394-5401 ◽

Cited By ~ 14

Author(s):

Emilie Lyautey ◽

Amandine Cournet ◽

Soizic Morin ◽

Stéphanie Boulêtreau ◽

Luc Etcheverry ◽

...

Keyword(s):

Stainless Steel ◽

Cyclic Voltammetry ◽

Oxygen Reduction ◽

Saturated Calomel Electrode ◽

Bacterial Strains ◽

Phenotypic Properties ◽

Content Type ◽

Population Scale ◽

River Biofilm ◽

Biofilm Development

ABSTRACTElectroactivity is a property of microorganisms assembled in biofilms that has been highlighted in a variety of environments. This characteristic was assessed for phototrophic river biofilms at the community scale and at the bacterial population scale. At the community scale, electroactivity was evaluated on stainless steel and copper alloy coupons used both as biofilm colonization supports and as working electrodes. At the population scale, the ability of environmental bacterial strains to catalyze oxygen reduction was assessed by cyclic voltammetry. Our data demonstrate that phototrophic river biofilm development on the electrodes, measured by dry mass and chlorophyllacontent, resulted in significant increases of the recorded potentials, with potentials of up to +120 mV/saturated calomel electrode (SCE) on stainless steel electrodes and +60 mV/SCE on copper electrodes. Thirty-two bacterial strains isolated from natural phototrophic river biofilms were tested by cyclic voltammetry. Twenty-five were able to catalyze oxygen reduction, with shifts of potential ranging from 0.06 to 0.23 V, cathodic peak potentials ranging from −0.36 to −0.76 V/SCE, and peak amplitudes ranging from −9.5 to −19.4 μA. These isolates were diversified phylogenetically (Actinobacteria,Firmicutes,Bacteroidetes, andAlpha-,Beta-, andGammaproteobacteria) and exhibited various phenotypic properties (Gram stain, oxidase, and catalase characteristics). These data suggest that phototrophic river biofilm communities and/or most of their constitutive bacterial populations present the ability to promote electronic exchange with a metallic electrode, supporting the following possibilities: (i) development of electrochemistry-based sensors allowingin situphototrophic river biofilm detection and (ii) production of microbial fuel cell inocula under oligotrophic conditions.

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Natural Disruption of Two Regulatory Networks in Serotype M3 Group A Streptococcus Isolates Contributes to the Virulence Factor Profile of This Hypervirulent Serotype

Infection and Immunity ◽

10.1128/iai.01639-13 ◽

2014 ◽

Vol 82 (5) ◽

pp. 1744-1754 ◽

Cited By ~ 24

Author(s):

Tram N. Cao ◽

Zhuyun Liu ◽

Tran H. Cao ◽

Kathryn J. Pflughoeft ◽

Jeanette Treviño ◽

...

Keyword(s):

Virulence Factor ◽

Regulatory Networks ◽

Molecular Mechanisms ◽

Group A Streptococcus ◽

Regulatory System ◽

Mrna Levels ◽

Bacterial Strains ◽

Content Type ◽

Small Regulatory Rna ◽

Group A

ABSTRACTDespite the public health challenges associated with the emergence of new pathogenic bacterial strains and/or serotypes, there is a dearth of information regarding the molecular mechanisms that drive this variation. Here, we began to address the mechanisms behind serotype-specific variation between serotype M1 and M3 strains of the human pathogenStreptococcus pyogenes(the group AStreptococcus[GAS]). Spatially diverse contemporary clinical serotype M3 isolates were discovered to contain identical inactivating mutations within genes encoding two regulatory systems that control the expression of important virulence factors, including the thrombolytic agent streptokinase, the protease inhibitor-binding protein-G-related α2-macroglobulin-binding (GRAB) protein, and the antiphagocytic hyaluronic acid capsule. Subsequent analysis of a larger collection of isolates determined that M3 GAS, since at least the 1920s, has harbored a 4-bp deletion in thefasCgene of thefasBCAXregulatory system and an inactivating polymorphism in therivRregulator-encoding gene. ThefasCandrivRmutations in M3 isolates directly affect the virulence factor profile of M3 GAS, as evident by a reduction in streptokinase expression and an enhancement of GRAB expression. Complementation of thefasCmutation in M3 GAS significantly enhanced levels of the small regulatory RNA FasX, which in turn enhanced streptokinase expression. Complementation of therivRmutation in M3 GAS restored the regulation ofgrabmRNA abundance but did not alter capsule mRNA levels. While important, thefasCandrivRmutations do not provide a full explanation for why serotype M3 strains are associated with unusually severe invasive infections; thus, further investigation is warranted.

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Characterization of a Novel Fructosyltransferase from Lactobacillus reuteri That Synthesizes High-Molecular-Weight Inulin and Inulin Oligosaccharides

Applied and Environmental Microbiology ◽

10.1128/aem.68.9.4390-4398.2002 ◽

2002 ◽

Vol 68 (9) ◽

pp. 4390-4398 ◽

Cited By ~ 104

Author(s):

S. A. F. T. van Hijum ◽

G. H. van Geel-Schutten ◽

H. Rahaoui ◽

M. J. E. C. van der Maarel ◽

L. Dijkhuizen

Keyword(s):

Molecular Weight ◽

High Molecular Weight ◽

Lactobacillus Reuteri ◽

Bacterial Strains ◽

Potential Health ◽

Isolation And Characterization ◽

A Cell ◽

Encoding Gene ◽

First Time

ABSTRACT Fructosyltransferase (FTF) enzymes produce fructose polymers (fructans) from sucrose. Here, we report the isolation and characterization of an FTF-encoding gene from Lactobacillus reuteri strain 121. A C-terminally truncated version of the ftf gene was successfully expressed in Escherichia coli. When incubated with sucrose, the purified recombinant FTF enzyme produced large amounts of fructo-oligosaccharides (FOS) with β-(2→1)-linked fructosyl units, plus a high-molecular-weight fructan polymer (>107) with β-(2→1) linkages (an inulin). FOS, but not inulin, was found in supernatants of L. reuteri strain 121 cultures grown on medium containing sucrose. Bacterial inulin production has been reported for only Streptococcus mutans strains. FOS production has been reported for a few bacterial strains. This paper reports the first-time isolation and molecular characterization of (i) a Lactobacillus ftf gene, (ii) an inulosucrase associated with a generally regarded as safe bacterium, (iii) an FTF enzyme synthesizing both a high molecular weight inulin and FOS, and (iv) an FTF protein containing a cell wall-anchoring LPXTG motif. The biological relevance and potential health benefits of an inulosucrase associated with an L. reuteri strain remain to be established.

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Discovery of a Conjugative Megaplasmid in Bifidobacterium breve

Applied and Environmental Microbiology ◽

10.1128/aem.02871-14 ◽

2014 ◽

Vol 81 (1) ◽

pp. 166-176 ◽

Cited By ~ 16

Author(s):

Francesca Bottacini ◽

Mary O'Connell Motherway ◽

Eoghan Casey ◽

Brian McDonnell ◽

Jennifer Mahony ◽

...

Keyword(s):

Genome Sequencing ◽

Dna Transfer ◽

Human Gut ◽

Genomic Features ◽

Content Type ◽

Bifidobacterium Breve ◽

Extrachromosomal Element ◽

Foreign Dna ◽

Transfer Apparatus

ABSTRACTBifidobacterium breveis a common and sometimes very abundant inhabitant of the human gut. Genome sequencing ofB. breveJCM 7017 revealed the presence of an extrachromosomal element, designated pMP7017 consisting of >190 kb, thus representing the first reported bifidobacterial megaplasmid.In silicocharacterization of this element revealed several genomic features supporting a stable establishment of the megaplasmid in its host, illustrated by predicted CRISPR-Cas functions that are known to protect the host against intrusion of foreign DNA. Interestingly, pMP7017 is also predicted to encode a conjugative DNA transfer apparatus and, consistent with this notion, we demonstrate here the conjugal transfer of pMP7017 to representative strains ofB. breveandB. longumsubsp.longum. We also demonstrate the presence of a megaplasmid with homology to pMP7017 in threeB. longumsubsp.longumstrains.

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Pathovar Transcriptomes

mSystems ◽

10.1128/msystems.00049-17 ◽

2017 ◽

Vol 2 (4) ◽

Cited By ~ 1

Author(s):

Amy Platenkamp ◽

Jay L. Mellies

Keyword(s):

Gene Expression ◽

Escherichia Coli ◽

Regulatory Networks ◽

Virulence Gene ◽

Model System ◽

Genomic Sequences ◽

Bacterial Strains ◽

Content Type ◽

Virulence Gene Expression ◽

Link Type

ABSTRACT Archetypal pathogenic bacterial strains are often used to elucidate regulatory networks of an entire pathovar, which encompasses multiple lineages and phylogroups. With enteropathogenic Escherichia coli (EPEC) as a model system, Hazen and colleagues (mSystems 6:e00024-17, 2017, https://doi.org/10.1128/mSystems.00024-17 ) used 9 isolates representing 8 lineages and 3 phylogroups to find that isolates with similar genomic sequences exhibit similarities in global transcriptomes under conditions of growth in medium that induces virulence gene expression, and they found variation among individual isolates. Archetypal pathogenic bacterial strains are often used to elucidate regulatory networks of an entire pathovar, which encompasses multiple lineages and phylogroups. With enteropathogenic Escherichia coli (EPEC) as a model system, Hazen and colleagues (mSystems 6:e00024-17, 2017, https://doi.org/10.1128/mSystems.00024-17 ) used 9 isolates representing 8 lineages and 3 phylogroups to find that isolates with similar genomic sequences exhibit similarities in global transcriptomes under conditions of growth in medium that induces virulence gene expression. They also found variation among individual isolates. Their work illustrates the importance of moving beyond observing regulatory phenomena of a limited number of regulons in a few archetypal strains, with the possibility of correlating clinical symptoms to key transcriptional pathways across lineages and phylogroups.

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Chitinophaga oryzae sp. nov., an epiphytic bacterium isolated from rice root surfaces

INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY ◽

10.1099/ijsem.0.004926 ◽

2021 ◽

Vol 71 (7) ◽

Author(s):

Nantawan Niemhom ◽

Chanwit Suriyachadkun ◽

Chokchai Kittiwongwattana

Keyword(s):

Type Species ◽

Rrna Gene ◽

Major Polar Lipid ◽

Bacterial Strains ◽

Respiratory Quinone ◽

Content Type ◽

Link Type ◽

Major Respiratory Quinone ◽

Phylogenomic Analyses ◽

Close Relatives

Two Gram-stain-negative, non-motile, rod-shaped bacterial strains were isolated from the surfaces of rice roots. They were designated as strains 1303T and 1310. Their colonies were circular, entire, opaque, convex and yellow. They were chitinase- and catalase-positive, reduced nitrate and grew at 16–37 °C (optimum, 30 °C), pH 5.0–10.0 (optimum, pH 7.0) and 0–2.0% NaCl (optimum, 1.0 %). Based on the 16S rRNA gene sequence analysis, they were classified as members of the genus Chitinophaga . Results of phylogenetic and phylogenomic analyses indicated that they formed a cluster with Chitinophaga eiseniae YC6729T, Chitinophaga qingshengii JN246T, Chitinophaga varians 10-7 W-9003T and Chitinophaga fulva G-6-1-13T. When the genomic sequences of strains 1303T and 1310 were compared with their close relatives, the average nucleotide identity and digital DNA–DNA hybridization values were below the cut-off levels. Phosphatidylethanolamine was the major polar lipid. MK-7 was the major respiratory quinone. iso-C15 : 0, C16 : 1 ω5c, iso-C17 : 0 3-OH and summed feature 3 (C16 : 1 ω7c/C16 : 1 ω6c) were the predominant fatty acids. Differential characteristics between both strains and their close relatives were also observed. Based on the distinctions in genotypic, phenotypic and chemotypic features, strains 1303T and 1310 represent members of a novel species of the genus Chitinophaga , for which the name Chitinophaga oryzae sp. nov. is proposed. The type strain is 1303T (=KACC 22075T=TBRC 12926T).

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Actinomyces marmotae sp. nov. and Actinomyces procaprae sp. nov. isolated from wild animals and reclassification of Actinomyces liubingyangii and Actinomyces tangfeifanii as Boudabousia liubingyangii comb. nov. and Boudabousia tangfeifanii comb. nov., respectively

INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY ◽

10.1099/ijsem.0.004696 ◽

2019 ◽

Vol 71 (3) ◽

Cited By ~ 16

Author(s):

Caixin Yang ◽

Yibo Bai ◽

Kui Dong ◽

Jing Yang ◽

Xin-He Lai ◽

...

Keyword(s):

Type Species ◽

Phylogenetic Analyses ◽

Brain Heart Infusion ◽

Tibet Plateau ◽

Rrna Gene ◽

Bacterial Strains ◽

Content Type ◽

Link Type ◽

Pr China ◽

Qinghai Tibet Plateau

Four Gram-stain-positive, catalase-negative, non-spore-forming, rod-shaped bacterial strains (zg-325T, zg329, dk561T and dk752) were isolated from the respiratory tract of marmot (Marmota himalayana) and the faeces of Tibetan gazelle (Procapra picticaudata) from the Qinghai-Tibet Plateau of PR China. The results of 16S rRNA gene sequence-based phylogenetic analyses indicated that strains zg-325T and dk561T represent members of the genus Actinomyces , most similar to Actinomyces denticolens DSM 20671T and Actinomyces ruminicola B71T, respectively. The DNA G+C contents of strains zg-325T and dk561T were 71.6 and 69.3 mol%, respectively. The digital DNA–DNA hybridization values of strains zg-325T and dk561T with their most closely related species were below the 70 % threshold for species demarcation. The four strains grew best at 35 °C in air containing 5 % CO2 on brain heart infusion (BHI) agar with 5 % sheep blood. All four strains had C18:1ω9c and C16:0 as the major cellular fatty acids. MK-8 and MK-9 were the major menaquinones in zg-325T while MK-10 was predominant in dk561T. The major polar lipids included diphosphatidylglycerol and phosphatidylinositol. On the basis of several lines of evidence from phenotypic and phylogenetic analyses, zg-325T and dk561T represent novel species of the genus Actinomyces , for which the name Actinomyces marmotae sp. nov. and Actinomyces procaprae sp. nov. are proposed. The type strains are zg-325T (=GDMCC 1.1724T=JCM 34091T) and dk561T (=CGMCC 4.7566T=JCM 33484T). We also propose, on the basis of the phylogenetic results herein, the reclassification of Actinomyces liubingyangii and Actinomyces tangfeifanii as Boudabousia liubingyangii comb. nov. and Boudabousia tangfeifanii comb. nov., respectively.

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