Adaptation to pH stress by Vibrio fischeri can affect its symbiosis with the Hawaiian bobtail squid (Euprymna scolopes)

Many microorganisms engaged in host-microbe interactions pendulate between a free-living phase and a host-affiliated stage. How adaptation to stress during the free-living phase affects host-microbe associations is unclear and understudied. To explore this topic, the symbiosis between Hawaiian bobtail squid (Euprymna scolopes) and the luminous bacterium Vibrio fischeri was leveraged for a microbial experimental evolution study. V. fischeri experienced adaptation to extreme pH while apart from the squid host. V. fischeri was serially passaged for 2000 generations to the lower and upper pH growth limits for this microorganism, which were pH 6.0 and 10.0, respectively. V. fischeri was also serially passaged for 2000 generations to vacillating pH 6.0 and 10.0. Evolution to pH stress both facilitated and impaired symbiosis. Microbial evolution to acid stress promoted squid colonization and increased bioluminescence for V. fischeri , while symbiont adaptation to alkaline stress diminished these two traits. Oscillatory selection to acid and alkaline stress also improved symbiosis for V. fischeri , but the facilitating effects were less than that provided by microbial adaptation to acid stress. In summary, microbial adaptation to harsh environments amid the free-living phase may impact the evolution of host-microbe interactions in ways that were not formerly considered.

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The Vibrio-Squid Symbiosis as a Model for Studying Interbacterial Competition

mSystems ◽

10.1128/msystems.00108-19 ◽

2019 ◽

Vol 4 (3) ◽

Author(s):

Alecia N. Septer

Keyword(s):

Vibrio Fischeri ◽

Experimental Methods ◽

Model System ◽

Bacterial Symbiont ◽

Euprymna Scolopes ◽

Content Type ◽

The Past ◽

Microbe Interactions ◽

Host Microbe Interactions ◽

Different Strains

ABSTRACT The symbiosis between Euprymna scolopes squid and its bioluminescent bacterial symbiont, Vibrio fischeri, is a valuable model system to study a natural, coevolved host-microbe association. Over the past 30 years, researchers have developed and optimized many experimental methods to study both partners in isolation and during symbiosis. These powerful tools, along with a strong foundational knowledge about the system, position the Vibrio-squid symbiosis at the forefront of host-microbe interactions because this system is uniquely suited to investigation of symbiosis from both host and bacterial perspectives. Moreover, the ability to isolate and characterize different strains of V. fischeri has revealed exciting new insights about how different genotypes evolve to compete for a host niche, including deploying interbacterial weapons early during host colonization. This Perspective explores how interbacterial warfare influences the diversity and spatial structure of the symbiotic population, as well as the possible effects that intraspecific competition might have on the host.

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A Small Molecule Coordinates Symbiotic Behaviors in a Host Organ

mBio ◽

10.1128/mbio.03637-20 ◽

2021 ◽

Vol 12 (2) ◽

Author(s):

Katherine E. Zink ◽

Denise A. Ludvik ◽

Phillip R. Lazzara ◽

Terry W. Moore ◽

Mark J. Mandel ◽

...

Keyword(s):

Mass Spectrometry ◽

Small Molecules ◽

Vibrio Fischeri ◽

Imaging Mass Spectrometry ◽

Light Organ ◽

Euprymna Scolopes ◽

Content Type ◽

Bacterial Luminescence ◽

Microbe Interactions ◽

Host Microbe Interactions

ABSTRACT The lifelong relationship between the Hawaiian bobtail squid Euprymna scolopes and its microbial symbiont Vibrio fischeri represents a simplified model system for studying microbiome establishment and maintenance. The bacteria colonize a dedicated symbiotic light organ in the squid, from which bacterial luminescence camouflages the host in a process termed counterillumination. The squid host hatches without its symbionts, which must be acquired from the ocean amidst a diversity of nonbeneficial bacteria, such that precise molecular communication is required for initiation of the specific relationship. Therefore it is likely there are specialized metabolites used in the light organ microenvironment to modulate these processes. To identify small molecules that may influence the establishment of this symbiosis, we used imaging mass spectrometry to analyze metabolite production in V. fischeri with altered biofilm production, which correlates directly to colonization capability in its host. “Biofilm-up” and “biofilm-down” mutants were compared to a wild-type strain, and ions that were more abundantly produced by the biofilm-up mutant were detected. Using a combination of structural elucidation and synthetic chemistry, one such signal was determined to be a diketopiperazine, cyclo(d-histidyl-l-proline). This diketopiperazine modulated luminescence in V. fischeri and, using imaging mass spectrometry, was directly detected in the light organ of the colonized host. This work highlights the continued need for untargeted discovery efforts in host-microbe interactions and showcases the benefits of the squid-Vibrio system for identification and characterization of small molecules that modulate microbiome behaviors. IMPORTANCE The complexity of animal microbiomes presents challenges to defining signaling molecules within the microbial consortium and between the microbes and the host. By focusing on the binary symbiosis between Vibrio fischeri and Euprymna scolopes, we have combined genetic analysis with direct imaging to define and study small molecules in the intact symbiosis. We have detected and characterized a diketopiperazine produced by strong biofilm-forming V. fischeri strains that was detectable in the host symbiotic organ, and which influences bacterial luminescence. Biofilm formation and luminescence are critical for initiation and maintenance of the association, respectively, suggesting that the compound may link early and later development stages, providing further evidence that multiple small molecules are important in establishing these beneficial relationships.

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Microbe Profile: Bdellovibrio bacteriovorus: a specialized bacterial predator of bacteria

Microbiology ◽

10.1099/mic.0.001043 ◽

2021 ◽

Vol 167 (4) ◽

Author(s):

Andrew L. Lovering ◽

R. Elizabeth Sockett

Keyword(s):

Type Species ◽

Free Living ◽

Prey Cell ◽

Bdellovibrio Bacteriovorus ◽

Content Type ◽

Link Type ◽

Attack Phase ◽

Future Potential ◽

Basic Biology ◽

The Way

Bdellovibrio bacteriovorus is an environmentally-ubiquitous bacterium that uses unique adaptations to kill other bacteria. The best-characterized strain, HD100, has a multistage lifestyle, with both a free-living attack phase and an intraperiplasmic growth and division phase inside the prey cell. Advances in understanding the basic biology and regulation of predation processes are paving the way for future potential therapeutic and bioremediation applications of this unusual bacterium.

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Multiple evolutionary origins reflect the importance of sialic acid transporters in the colonization potential of bacterial pathogens and commensals

Microbial Genomics ◽

10.1099/mgen.0.000614 ◽

2021 ◽

Vol 7 (6) ◽

Author(s):

Emmanuele Severi ◽

Michelle Rudden ◽

Andrew Bell ◽

Tracy Palmer ◽

Nathalie Juge ◽

...

Keyword(s):

Phylogenetic Analysis ◽

Sialic Acid ◽

Sialic Acids ◽

Content Type ◽

Link Type ◽

Evolutionary Origins ◽

Mucosal Surfaces ◽

Colonization Potential ◽

Microbe Interactions ◽

Host Microbe Interactions

Located at the tip of cell surface glycoconjugates, sialic acids are at the forefront of host–microbe interactions and, being easily liberated by sialidase enzymes, are used as metabolites by numerous bacteria, particularly by pathogens and commensals living on or near diverse mucosal surfaces. These bacteria rely on specific transporters for the acquisition of host-derived sialic acids. Here, we present the first comprehensive genomic and phylogenetic analysis of bacterial sialic acid transporters, leading to the identification of multiple new families and subfamilies. Our phylogenetic analysis suggests that sialic acid-specific transport has evolved independently at least eight times during the evolution of bacteria, from within four of the major families/superfamilies of bacterial transporters, and we propose a robust classification scheme to bring together a myriad of different nomenclatures that exist to date. The new transporters discovered occur in diverse bacteria, including Spirochaetes , Bacteroidetes , Planctomycetes and Verrucomicrobia , many of which are species that have not been previously recognized to have sialometabolic capacities. Two subfamilies of transporters stand out in being fused to the sialic acid mutarotase enzyme, NanM, and these transporter fusions are enriched in bacteria present in gut microbial communities. Our analysis supports the increasing experimental evidence that competition for host-derived sialic acid is a key phenotype for successful colonization of complex mucosal microbiomes, such that a strong evolutionary selection has occurred for the emergence of sialic acid specificity within existing transporter architectures.

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Investigation of the polyamine biosynthetic and transport capability of Streptococcus agalactiae: the non-essential PotABCD transporter

Microbiology ◽

10.1099/mic.0.001124 ◽

2021 ◽

Vol 167 (12) ◽

Author(s):

Sarah Khazaal ◽

Rim Al Safadi ◽

Dani Osman ◽

Aurélia Hiron ◽

Philippe Gilot

Keyword(s):

Oxidative Stress ◽

Streptococcus Agalactiae ◽

Type Species ◽

Physiological Stress ◽

Acid Stress ◽

Phenotypic Traits ◽

Growth Media ◽

Content Type ◽

Peptidoglycan Biosynthesis ◽

Link Type

Polyamines constitute a group of organic polycations positively charged at physiological pH. They are involved in a large variety of biological processes, including the protection against physiological stress. In this study, we show that the genome of Streptococcus agalactiae , a commensal bacterium of the intestine and the vagina and one of the most common agents responsible of neonate infections, does not encode proteins homologous to the specific enzymes involved in the known polyamine synthetic pathways. This lack of biosynthetic capability was verified experimentally by TLC analysis of the intracellular content of S. agalactiae grown in the absence of polyamines. However, similar analyses showed that the polyamines spermidine, spermine and putrescine can be imported from the growth media into the bacteria. We found that all strains of S. agalactiae possess the genes encoding the polyamine ABC transporter PotABCD. We demonstrated that these genes form an operon with folK, a gene involved in folate biosynthesis, murB, a gene involved in peptidoglycan biosynthesis, and with clc, a gene encoding a Cl−/H+ antiporter involved in resistance to acid stress in Escherichia coli . Transcription of the potABCD operon is induced by peroxide-induced oxidative stress but not by acidic stress. Spermidine and spermine were found to be inducers of potABCD transcription at pH 7.4 whereas putrescine induces this expression only during peroxide-induced oxidative stress. Using a deletion mutant of potABCD, we were nevertheless unable to associate phenotypic traits to the PotABCD transporter, probably due to the existence of one or more as yet identified transporters with a redundant action.

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Niche-Specific Impact of a Symbiotic Function on the Persistence of Microbial Symbionts within a Natural Host

Applied and Environmental Microbiology ◽

10.1128/aem.01770-16 ◽

2016 ◽

Vol 82 (19) ◽

pp. 5990-5996 ◽

Cited By ~ 7

Author(s):

Subhash C. Verma ◽

Tim Miyashiro

Keyword(s):

Vibrio Fischeri ◽

Fundamental Aspect ◽

Light Organ ◽

Content Type ◽

Host Environment ◽

Microbe Interactions ◽

Host Microbe Interactions ◽

Microbial Symbionts ◽

Function Relationship ◽

The Impact

ABSTRACTHow the function of microbial symbionts is affected by their population/consortium structure within a host remains poorly understood. The symbiosis established betweenEuprymna scolopesandVibrio fischeriis a well-characterized host-microbe association in which the function and structure ofV. fischeripopulations within the host are known:V. fischeripopulations produce bioluminescence from distinct crypt spaces within a dedicated host structure called the light organ. Previous studies have revealed that luminescence is required forV. fischeripopulations to persist within the light organ and that deletion of theluxgene locus, which is responsible for luminescence inV. fischeri, leads to a persistence defect. In this study, we investigated the impact of bioluminescence onV. fischeripopulation structure within the light organ. We report that the persistence defect is specific to crypt I, which is the most developmentally mature crypt space within the nascent light organ. This result provides insight into the structure/function relationship that will be useful for future mechanistic studies of squid-Vibriosymbiosis. In addition, our report highlights the potential impact of the host developmental program on the spatiotemporal dynamics of host-microbe interactions.IMPORTANCEMetazoan development and physiology depend on microbes. The relationship between the symbiotic function of microbes and their spatial structure within the host environment remains poorly understood. Here we demonstrate, using a binary symbiosis, that the host requirement for the symbiotic function of the microbial symbiont is restricted to a specific host environment. Our results also suggest a link between microbial function and host development that may be a fundamental aspect of the more complex host-microbe interactions.

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Bactericidal Permeability-Increasing Proteins Shape Host-Microbe Interactions

mBio ◽

10.1128/mbio.00040-17 ◽

2017 ◽

Vol 8 (2) ◽

Cited By ~ 15

Author(s):

Fangmin Chen ◽

Benjamin C. Krasity ◽

Suzanne M. Peyer ◽

Sabrina Koehler ◽

Edward G. Ruby ◽

...

Keyword(s):

Antimicrobial Activity ◽

Vibrio Fischeri ◽

Molecular Characteristics ◽

Light Organ ◽

Euprymna Scolopes ◽

Lipopolysaccharide Binding Protein ◽

Ambient Seawater ◽

Microbe Interactions ◽

Acidic Conditions ◽

Host Microbe Interactions

ABSTRACT We characterized bactericidal permeability-increasing proteins (BPIs) of the squid Euprymna scolopes , EsBPI2 and EsBPI4. They have molecular characteristics typical of other animal BPIs, are closely related to one another, and nest phylogenetically among invertebrate BPIs. Purified EsBPIs had antimicrobial activity against the squid’s symbiont, Vibrio fischeri , which colonizes light organ crypt epithelia. Activity of both proteins was abrogated by heat treatment and coincubation with specific antibodies. Pretreatment under acidic conditions similar to those during symbiosis initiation rendered V. fischeri more resistant to the antimicrobial activity of the proteins. Immunocytochemistry localized EsBPIs to the symbiotic organ and other epithelial surfaces interacting with ambient seawater. The proteins differed in intracellular distribution. Further, whereas EsBPI4 was restricted to epithelia, EsBPI2 also occurred in blood and in a transient juvenile organ that mediates hatching. The data provide evidence that these BPIs play different defensive roles early in the life of E. scolopes , modulating interactions with the symbiont. IMPORTANCE This study describes new functions for bactericidal permeability-increasing proteins (BPIs), members of the lipopolysaccharide-binding protein (LBP)/BPI protein family. The data provide evidence that these proteins play a dual role in the modulation of symbiotic bacteria. In the squid-vibrio model, these proteins both control the symbiont populations in the light organ tissues where symbiont cells occur in dense monoculture and, concomitantly, inhibit the symbiont from colonizing other epithelial surfaces of the animal.

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Faecalicoccus acidiformans gen. nov., sp. nov., isolated from the chicken caecum, and reclassification of Streptococcus pleomorphus (Barnes et al. 1977), Eubacterium biforme (Eggerth 1935) and Eubacterium cylindroides (Cato et al. 1974) as Faecalicoccus pleomorphus comb. nov., Holdemanella biformis gen. nov., comb. nov. and Faecalitalea cylindroides gen. nov., comb. nov., respectively, within the family Erysipelotrichaceae

INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY ◽

10.1099/ijs.0.064626-0 ◽

2014 ◽

Vol 64 (Pt_11) ◽

pp. 3877-3884 ◽

Cited By ~ 50

Author(s):

Celine De Maesschalck ◽

Filip Van Immerseel ◽

Venessa Eeckhaut ◽

Siegrid De Baere ◽

Margo Cnockaert ◽

...

Keyword(s):

16S Rrna ◽

16S Rrna Gene ◽

Type Species ◽

Gene Sequence ◽

Sequence Similarity ◽

16S Rrna Gene Sequence ◽

Rrna Gene ◽

Rrna Gene Sequence ◽

Content Type ◽

Link Type

Strains LMG 27428T and LMG 27427 were isolated from the caecal content of a chicken and produced butyric, lactic and formic acids as major metabolic end products. The genomic DNA G+C contents of strains LMG 27428T and LMG 27427 were 40.4 and 38.8 mol%. On the basis of 16S rRNA gene sequence similarity, both strains were most closely related to the generically misclassified Streptococcus pleomorphus ATCC 29734T. Strain LMG 27428T could be distinguished from S. pleomorphus ATCC 29734T based on production of more lactic acid and less formic acid in M2GSC medium, a higher DNA G+C content and the absence of activities of acid phosphatase and leucine, arginine, leucyl glycine, pyroglutamic acid, glycine and histidine arylamidases, while strain LMG 27428 was biochemically indistinguishable from S. pleomorphus ATCC 29734T. The novel genus Faecalicoccus gen. nov. within the family Erysipelotrichaceae is proposed to accommodate strains LMG 27428T and LMG 27427. Strain LMG 27428T ( = DSM 26963T) is the type strain of Faecalicoccus acidiformans sp. nov., and strain LMG 27427 ( = DSM 26962) is a strain of Faecalicoccus pleomorphus comb. nov. (type strain LMG 17756T = ATCC 29734T = DSM 20574T). Furthermore, the nearest phylogenetic neighbours of the genus Faecalicoccus are the generically misclassified Eubacterium cylindroides DSM 3983T (94.4 % 16S rRNA gene sequence similarity to strain LMG 27428T) and Eubacterium biforme DSM 3989T (92.7 % 16S rRNA gene sequence similarity to strain LMG 27428T). We present genotypic and phenotypic data that allow the differentiation of each of these taxa and propose to reclassify these generically misnamed species of the genus Eubacterium formally as Faecalitalea cylindroides gen. nov., comb. nov. and Holdemanella biformis gen. nov., comb. nov., respectively. The type strain of Faecalitalea cylindroides is DSM 3983T = ATCC 27803T = JCM 10261T and that of Holdemanella biformis is DSM 3989T = ATCC 27806T = CCUG 28091T.

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Pseudoseohaeicola caenipelagi gen. nov., sp. nov., isolated from a tidal flat

INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY ◽

10.1099/ijs.0.000182 ◽

2015 ◽

Vol 65 (Pt_6) ◽

pp. 1819-1824 ◽

Cited By ~ 15

Author(s):

Sooyeon Park ◽

Ji-Min Park ◽

Chul-Hyung Kang ◽

Song-Gun Kim ◽

Jung-Hoon Yoon

Keyword(s):

16S Rrna ◽

16S Rrna Gene ◽

Tidal Flat ◽

Type Strain ◽

Type Species ◽

Phylogenetic Trees ◽

Sequence Similarity ◽

Rrna Gene ◽

Content Type ◽

Link Type

A Gram-stain-negative, non-motile, aerobic and pleomorphic bacterium, designated BS-W13T, was isolated from a tidal flat on the South Sea, South Korea, and its taxonomic position was investigated using a polyphasic approach. Strain BS-W13T grew optimally at 25 °C, at pH 7.0–8.0 and in the presence of 1.0–2.0 % (w/v) NaCl. Neighbour-joining and maximum-parsimony phylogenetic trees based on 16S rRNA gene sequences showed that strain BS-W13T clustered with the type strain of Seohaeicola saemankumensis , showing the highest sequence similarity (95.96 %) to this strain. Strain BS-W13T exhibited 16S rRNA gene sequence similarity values of 95.95, 95.91, 95.72 and 95.68 % to the type strains of Sulfitobacter donghicola , Sulfitobacter porphyrae , Sulfitobacter mediterraneus and Roseobacter litoralis , respectively. Strain BS-W13T contained Q-10 as the predominant ubiquinone and C18 : 1ω7c as the major fatty acid. The polar lipid profile of strain BS-W13T, containing phosphatidylcholine, phosphatidylglycerol, phosphatidylethanolamine, one unidentified aminolipid and one unidentified lipid as major components, was distinguishable from those of some phylogenetically related taxa. The DNA G+C content of strain BS-W13T was 58.1 mol%. The phylogenetic data and differential chemotaxonomic and other phenotypic properties revealed that strain BS-W13T constitutes a novel genus and species within family Rhodobacteraceae of the class Alphaproteobacteria , for which the name Pseudoseohaeicola caenipelagi gen. nov., sp. nov. is proposed. The type strain is BS-W13T ( = KCTC 42349T = CECT 8724T).

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Litorilinea aerophila gen. nov., sp. nov., an aerobic member of the class Caldilineae , phylum Chloroflexi , isolated from an intertidal hot spring

INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY ◽

10.1099/ijs.0.044115-0 ◽

2013 ◽

Vol 63 (Pt_3) ◽

pp. 1149-1154 ◽

Cited By ~ 22

Author(s):

Varsha Kale ◽

Snædís H. Björnsdóttir ◽

Ólafur H. Friðjónsson ◽

Sólveig K. Pétursdóttir ◽

Sesselja Ómarsdóttir ◽

...

Keyword(s):

Type Species ◽

Hot Spring ◽

Sequence Similarity ◽

Rrna Gene ◽

Content Type ◽

Phenotypic Differences ◽

Link Type ◽

Fermentative Growth ◽

Distinct Lineage ◽

Ph Range

A thermophilic, aerobic, Gram-stain-negative, filamentous bacterium, strain PRI-4131T, was isolated from an intertidal hot spring in Isafjardardjup, NW Iceland. The strain grew chemo-organotrophically on various carbohydrates. The temperature range for growth was 40–65 °C (optimum 55 °C), the pH range was pH 6.5–9.0 (optimum pH 7.0) and the NaCl range was 0–3 % (w/v) (optimum 0.5 %). Phylogenetic analysis based on 16S rRNA gene sequences revealed that strain PRI-4131T represented a distinct lineage within the class Caldilineae of the phylum Chloroflexi. The highest levels of sequence similarity, about 91 %, were with Caldilinea aerophila STL-6-O1T and Caldilinea tarbellica D1-25-10-4T. Fermentative growth was not observed for strain PRI-4131T, which, in addition to other characteristics, distinguished it from the two Caldilinea species. Owing to both phylogenetic and phenotypic differences from the described members of the class Caldilineae , we propose to accommodate strain PRI-4131T in a novel species in a new genus, Litorilinea aerophila gen. nov., sp. nov. The type strain of Litorilinea aerophila is PRI-4131T ( = DSM 25763T = ATCC BAA-2444T).

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