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Proposal of Cobetia marina gen. nov., comb. nov., within the family Halomonadaceae, to include the species Halomonas marina.

At present the family Halomonadaceae consists of four genera and the taxonomic status of all species included in these genera is not equally supported by phylogenetic evidence. Whereas Zymobacter and Carnimonas contain one single species each and form the deeper branch of the family, the genus Halomonas contains currently 22 species, with a maximum 16S/23S rRNA sequence divergence greater than it could be expected for species of the same genus. In addition, we have witnessed during last years an increase in the number of new species within this group, which makes even more necessary a taxonomic rearrangement. In a previous study (Arahal et al., 2002) we evaluated the phylogenetic status of the family Halomonadaceae based on 23S and 16S rDNA sequence analyses and mentioned that Halomonas marina could eventually be assigned to a new genus. In this study we have emended the description of this species, including new features and propose its placement in a new genus, Cobetia gen. nov. within the family Halomonadaceae. The type strain of Cobetia marina is ATCC 25374T (= DSM 4741T). Further discussion on the phylogeny of the family Halomonadaceae is provided taking into account the most recent changes.

Base Sequence↗

Phylogeny of the family Halomonadaceae based on 23S and 165 rDNA sequence analyses.

In this study, we have evaluated the phylogenetic status of the family Halomonadaceae, which consists of the genera Halomonas, Chromohalobacter and Zymobacter, by comparative 23S and 16S rDNA analyses. The genus Halomonas illustrates very well a situation that occurs often in bacterial taxonomy. The use of phylogenetic tools has permitted the grouping of several genera and species believed to be unrelated according to conventional taxonomic techniques. In addition, the number of species of the genus Halomonas has increased as a consequence of new descriptions, particularly during the last few years, but their features are too heterogeneous to justify their placement in the same genus and, therefore, a re-evaluation seems necessary. We have determined the complete sequences (about 2900 bases) of the 23S rDNA of 18 species of the genera Halomonas and Chromohalobacter and resequenced the complete 16S rDNA sequences of seven species of Halomonas. The results of our analysis show that two phylogenetic groups (respectively containing five and seven species) can be distinguished within the genus Halomonas. Six other species cannot be assigned to either of the above-mentioned groups. Furthermore, Halomonas marina forms a separate branch at a deeper level than the other species of the genus Halomonas, which suggests that it should be ascribed to a separate genus. The genus Chromohalobacter forms a monophyletic group constituted by Chromohalobacter marismortui, the recently reclassified species Chromohalobacter canadensis and Chromohalobacter israelensis and the recently proposed species Chromohalobacter salexigens. Finally, we propose to include the genus Carnimonas, with its single species Carnimonas nigrificans, in the family Halomonadaceae.

Animals↗

Genetic tools for the manipulation of moderately halophilic bacteria of the family Halomonadaceae.

Moderately halophilic bacteria of the family Halomonadaceae (Halomonas, Chromohalobacter, and Zymobacter) have promising applications in biotechnology as a source of compatible solutes (stabilizers of biomolecules and cells), salt-tolerant enzymes, biosurfactants, and extracellular polysaccharides, among other products. In addition, they offer a number of advantages to be used as cell factories, alternative to conventional prokaryotic hosts like E. coli or Bacillus, for the production of recombinant proteins: (1) their high salt tolerance decreases to a minimum the necessity for aseptic conditions, resulting in cost-reducing conditions; (2) they are very easy to grow and maintain in the laboratory, and their nutritional requirements are simple; and (3) the majority can use a large range of compounds as a sole carbon and energy source. In this decade, the efforts of our group and others have made possible the genetic manipulation of this bacterial group. In this review, the most relevant tools are described, with emphasis given to cloning vectors, genetic exchange mechanisms, mutagenesis approaches, and reporter genes. Due to its relevance for genetic studies, complementary sections describing the influence of salinity on the susceptibility of moderately halophilic bacteria to antimicrobials, as well as the growth media most routinely used, culture conditions, and nucleic acid isolation procedures for these microorganisms, are included.

Culture Media↗

Polyamine distribution patterns within the families Aeromonadaceae, Vibrionaceae, Pasteurellaceae, and Halomonadaceae, and related genera of the gamma subclass of the Proteobacteria.

Polyamines of the four families and the five related genera within the gamma subclass of the class Proteobacteria were analyzed by HPLC with the objective of developing a chemotaxonomic system. The production of putrescine, diaminopropane, cadaverine, and agmatine are not exactly correlated to the phylogenetic genospecies within 36 strains of the genus Aeromonas (the family Aeromonadaceae) lacking in triamines. The occurrence of norspermidine was limited but not ubiquitous within the family Vibrionaceae, including 20 strains of Vibrio, Listonella, Photobacterium, and Salinivibrio. Spermidine was not substituted for the absence of norspermidine in the family. Agmatine was detected only in Photobacterium. Salinivibrio and some strains of Vibrio were devoid of polyamines. Vibrio ("Moritella") marinus contained cadaverine. Within the family Pasteurellaceae, Haemophilus contained cadaverine only and Actinobacillus contained no polyamine. Halomonas, Chromohalobacter, and Zymobacter, belonging to the family Halomonadaceae, ubiquitously contained spermidine and sporadically cadaverine and agmatine. Shewanella contained putrescine and cadaverine; Alteromonas macleodii, putrescine, 2-hydroxyputrescine, cadaverine, 2-hydroxyspermidine, and spermidine; Pseudoalteromonas, putrescine, cadaverine, and spermidine; Marinobacter, spermidine; and Marinomonas, putrescine and spermidine. Their polyamine profiles serve as a chemotaxonomic marker within the gamma subclass.

Journal Article↗

Phylogenetic relationships between some members of the genera Deleya, Halomonas, and Halovibrio.

The genera Halomonas and Deleya, which constitute the family Halomonadaceae, are difficult to differentiate on the basis of phenotypic and chemotaxonomic attributes. DNA-rRNA hybridization studies have indicated that some Halomonas spp. have the same level of relationship to the type species of the genus Deleya as some Deleya spp. A phylogenetic analysis of the 16S rRNA sequences of seven members of the Halomonadaceae indicated that the members of the genera Halomonas and Deleya do not form separate monophyletic subgroups, confirming the lack of any phylogenetic support for retention of these taxa as separate genera. A phylogenetic analysis of the 16S rRNA sequence of Halovibrio variabilis confirmed that this species belongs in the Halomonadaceae. All of the members of the Halomonadaceae examined and Halovibrio variabilis possess a cytosine residue at position 486 (Escherichia coli numbering), which is an extremely rare attribute among the prokaryotes and has been reported in only one other species, Listonella anguillarum. Several other signature characteristics which define this group in the gamma subclass of the Proteobacteria are identified. The Jukes-Cantor distances between members of the family Halomonadaceae, including Halovibrio variabilis, range from 0.086 to 0.000 (the levels of similarity between the 16S rRNA sequences range from 92.6 to 100%). The members of the genera Halomonas, Deleya, and Halovibrio form a monophyletic group and share common chemotaxonomic and phenotypic characteristics. Subgroups containing members of the genera Halomonas, Deleya, and Halovibrio cannot be resolved on the basis of phylogenetic, chemotaxonomic, or phenotypic data. Our data indicate that the members of the genera Halomonas, Deleya, and Halovibrio should be united in a single genus.

Biological Evolution↗

Halomonas magadii sp. nov., a new member of the genus Halomonas, isolated from a soda lake of the East African Rift Valley.

A number of novel alkaliphilic organotrophic bacteria have been isolated from several saline and alkaline East African soda lakes. The new isolates grow at pH values between 7.0 and 11.0, with pH optima for growth between 9.0 and 10.0. Growth occurs at total salts concentration between 0% and 20% (w/v) with optimum at 0%-7% (w/v). Phylogenetic analyses based on 16S rDNA sequence comparison indicate that these isolates are related (>96% similarity) to members of the Halomonadaceae within the gamma-3 subdivision of the Proteobacteria. These analyses indicate that existing species within the Halomonadaceae fell within three main groups, one group comprising the type species of Halomonas, Halomonas elongata, and a number of other known species including one soda lake isolate. A second group constituting most of the remaining known species of Halomonas and related Chromohalobacter spp. includes 3 soda lake isolates with high DNA-DNA homologies. The third group included Halomonas halodenitrificans, Halomonas desiderata, Halomonas cupida, and 13 soda lake isolates. Phenotypic comparisons indicated that the majority of soda lake strains shared similar morphological, phenotypic, and chemotaxonomic properties to known strains of Halomonas but grew under alkaline conditions. The 3 soda lake isolates with high DNA-DNA homologies were, however, significantly different in antibiotic sensitivity pattern and in the utilization of several substrates, were unable to reduce nitrite, and showed low DNA-DNA homologies with known halomonads in the same group. We propose that these isolates comprise a new species of the genus Halomonas that we name Halomonas magadii sp. nov. The type strain is strain 21 MI (NCIMB 13595).

Africa↗

Phylogenetic inferences and taxonomic consequences of 16S ribosomal DNA sequence comparison of Chromohalobacter marismortui, Volcaniella eurihalina, and Deleya salina and reclassification of V. eurihalina as Halomonas eurihalina comb. nov.

The phylogenetic positions of the moderately halophilic bacteria Chromohalobacter marismortui, Volcaniella eurihalina, and Deleya salina were determined by PCR amplification of rRNA genes and direct sequencing. The resulting data were compared with data for other bacteria obtained from 16S rRNA sequence databases. C. marismortui, V. eurihalina, and D. salina clustered phylogenetically within the gamma subclass of the Proteobacteria and are closely related to other species on the Halomonas-Deleya branch. C. marismortui belongs in the family Halomonadaceae and has the characteristic 16S rRNA signatures defined for this family, including the distinctive cytosine residue at position 486 found in all members of the Halomonadaceae. V. eurihalina is closely related to the type species of the genus Halomonas, Halomonas elongata, and we formally propose that V. eurihalina should be transferred to the genus Halomonas as Halomonas eurihalina comb. nov. The type strain of this species is strain F9-6 (= ATCC 49336). D. salina is not as closely related to other species belonging to the Halomonas-Deleya complex, but is more closely related to Halomonas elongata than to Deleya aquamarina, the type species of the genus Deleya. A polyphasic approach will be necessary to determine the natural taxonomic positions of the species belonging to the genera Halomonas and Deleya, as well as C. marismortui, V. eurihalina, Halovibrio variabilis, and Paracoccus halodenitrificans.

Base Sequence↗

Halomonas glaciei sp. nov. isolated from fast ice of Adelie Land, Antarctica.

Eleven psychrophilic bacteria were isolated from a solid layer of fast ice in the middle of Pointe-Geologie Archipelago, Adelie Land, Antarctica. The 11 isolates based on the phenotypic characteristics, chemotaxonomic and phylogenetic analysis have been identified as members of the genus Halomonas. All the isolates at the 16S rDNA sequence level were identical, possessed the 15 conserved nucleotides of the family Halomonadaceae and four nucleotides of the genus Halomonas. Therefore, the 16S rDNA sequence of DD 39 was used for calculating the evolutionary distances and for phylogenetic analysis. It was observed that DD 39 formed a robust cluster with H. variabilis, from which it differed by 0.7%. Further DNA-DNA hybridization studies indicated low DNA-DNA homology (15%) between H. variabilis and DD 39. Between the 11 Antarctic isolates the homology was >85%. In addition it was observed that DD 39 was different from H. variabilis in that it was psychrophilic, could tolerate only up to 15% sodium chloride, could not hydrolyse esculin, could not reduce nitrate, was urease negative, could not utilize glycerol as a carbon source, and was resistant to ampicillin and erythromycin and sensitive to nalidixic acid. In addition, it also exhibited distinct differences with respect to high content of C(16:1) and low levels of cyclo-C(17:0) and cyclo-C(19:0). DD 39 also differed from all the other reported species of Halomonas with respect to many phenotypic characteristics. It is proposed therefore that DD 39 should be placed in the genus Halomonas as a new species that is Halomonas glaciei. The type strain of H. glaciei is DD 39(T) (MTCC 4321; JCM 11692).

Antarctic Regions↗

Reevaluating the classification of Paracoccus halodenitrificans with sequence comparisons of 16S ribosomal DNA.

The results of phylogenetic analysis in which 16S ribosomal DNA sequences were compared confirmed previous chemotaxonomic data which suggested that Paracoccus halodenitrificans is inappropriately placed in the genus Paracoccus, which belongs in the alpha subclass of the Proteobacteria. P. halodenitrificans should be placed in the family Halomonadaceae, which belongs in the gamma subclass of the Proteobacteria.

DNA, Ribosomal↗

Phylogenetic analysis of psychrophilic bacteria isolated from the Japan Trench, including a description of the deep-sea species Psychrobacter pacificensis sp. nov.

Phylogenetic positions of psychrophilic bacteria isolated from the Japan Trench were determined by sequencing analysis of PCR-amplified bacterial small subunit (16S) rRNA genes. Between surface and deep-sea psychrophiles, distinct positions clearly differed within the gamma-Proteobacteria. In phylogenetic analysis using neighbour-joining, maximum-parsimony and maximum-likelihood, strains from surface seawater were inferred to be located in the Halomonas aquamarina-meridiana clade within the family Halomonadaceae. Strains from deep seawater (5000-6000 m), however, formed a novel monophyletic clade within the Moraxella-Psychrobacter branch in the family Moraxellaceae, showing separation from terrestrial and Antarctic relatives. These deep-sea strains were also discriminated from other known Psychrobacter species in phenotype, e.g. limited growth in the absence of NaCl (optimum at about 3% NaCl), positive urease activity, acid production from xylose and arabinose, and the presence of multiple fimbriae. DNA relatedness values among six deep-sea strains were > 85% in DNA-DNA hybridization experiments and > 98% in aligned 16S rDNA sequences. From this evidence, a new species, Psychrobacter pacificensis, is proposed for these deep-sea psychrophiles; the type strain of Psychrobacter pacificensis is strain NIBH P2K6T (= IFO 16270T). Occurrence of psychrobacters in cold Japan Trench deep seawater and at the Antarctic sea surface suggests that deep-sea bacterial habitation and evolution have been mediated by global deep-ocean circulation linked to the sinking of cooled seawater in polar regions.

Cold Temperature↗

Re-examining the 16S rDNA sequence of Halomonas salina.

Previous reports of 16S rDNA sequencing of members of the family Halomonadaceae Franzmann et al. 1989 include two different sequences that were both attributed to the type strain of Halomonas salina (Valderrama et al. 1991) Dobson and Franzmann 1996 (basonym Deleya salina Valderrama et al. 1991). The two sequences are sufficiently different for them to belong to two different species within the genus Halomonas. In order to determine which of the two sequences corresponded to that of the type strain of Halomonas salina, the designated type strains of this species were obtained from the ATCC and the DSMZ. It was possible to show that only one of the previous sequences corresponded to the sequences obtained from DSMZ 5928T and ATCC 49509T.

DNA, Bacterial↗

Halomonas marisflavae sp. nov., a halophilic bacterium isolated from the Yellow Sea in Korea.

A halophilic Gram-negative bacterial strain, SW32T, which was isolated from a sample from the Yellow Sea of Korea, was subjected to a polyphasic taxonomic study. This organism grew optimally in the presence of 0.5-12% NaCl. On the basis of phenotypic and phylogenetic data, strain SW32T appeared to be a member of the genus Halomonas. Strain SW32T formed a distinct evolutionary lineage within the phylogenetic clade comprising Halomonas species and the genera Zymobacter and Carnimonas. The 16S rDNA sequence of strain SW32T contains 19 signature characteristics of the genus Halomonas and the family Halomonadaceae. Strain SW32T possessed a single polar flagellum, ubiquinone-9 as the predominant respiratory lipoquinone and C18:1, C16:0 and C16:1 omega7c and/or iso-C15:0 20H as the major fatty acids. The DNA G+C content was 59 mol%. Levels of 16S rDNA similarity between strain SW32T and the type strains of all validly described Halomonas species were 92.0-93.8%. Strain SW32T exhibited 16S rDNA similarity values of 92.7% to Zymobacter palmae IAM 14233T and 91.6% to Carnimonas nigrificans CECT 4437T. These data indicate that strain SW32T was related enough to members of the genus Halomonas to be placed as a new species within that genus. Therefore the name Halomonas marisflavae sp. nov. is proposed for strain SW32T. The type strain of the new species is strain SW32T (= KCCM 80003T = JCM 10873T).

DNA, Ribosomal↗

Transfer of Halomonas canadensis and Halomonas israelensis to the genus Chromohalobacter as Chromohalobacter canadensis comb. nov. and Chromohalobacter israelensis comb. nov..

16S rRNA gene sequence comparisons and DNA-DNA hybridization data support the conclusion that two species previously described as members of the genus Halomonas, Halomonas israelensis and Halomonas canadensis, should be placed in the genus Chromohalobacter. Both H. israelensis ATCC 43985T (= Ba1T) and H. canadensis ATCC 43984T (= NRCC 41227T) have been used extensively for physiological studies for many years; nevertheless, they were not named and classified taxonomically until quite recently. Their phenotypic resemblance (at least 65% Jaccard similarity) to some members of the genus Halomonas and the degree of DNA-DNA relatedness (lower than 60%) to other described species of this genus permitted the conclusion that they were distinct species belonging to the genus Halomonas. In this study, the 16S rDNA of both species has been sequenced completely and found to share higher similarity to the available sequences of the moderately halophilic bacterium Chromohalobacter marismortui than to sequences of members of the genus Halomonas. C. marismortui is the sole species of the genus Chromohalobacter, also included in the family Halomonadaceae, and shares many phenotypic features with H. canadensis and H. israelensis. It is proposed that the two species should be renamed as Chromohalobacter canadensis comb. nov. and Chromohalobacter israelensis comb. nov. An emended description of the genus Chromohalobacter is given in order to include the features of these two species.

DNA, Bacterial↗

Degradation of 2,4-dichlorophenoxyacetic acid by haloalkaliphilic bacteria.

Three 2,4-dichlorophenoxyacetic acid (2,4-D)-degrading bacterial isolates were obtained from the highly saline and alkaline Alkali Lake site in southwestern Oregon contaminated with 2,4-D production wastes. While similar in most respects, the three isolates differed significantly in 2,4-D degradation rates, with the most active strain, I-18, demonstrating an ability to degrade up to 3000 mg 2,4-D I-1 in 3 d. This strain was well adapted to the extreme environment from which it was isolated, growing optimally on 2,4-D at pH 8.4-9.4 and at sodium ion concentrations of 0.6-1.0 M. According to its optimum salt concentration and pH for growth, this isolate was a moderately halophilic, alkaliphilic bacterium. The 16S RNA gene sequence (303 nt) was identical for all three isolates and most closely resembled those of the moderately halophilic eubacteria of the family Halomonadaceae (91% identity). Biochemical and genetic examination revealed strain I-18 utilizes the same 2,4-D degradation pathway as most of the 2,4-D-degrading bacteria from non-extreme environments. Hybridization data and comparison of the partial sequences of the tfdA gene from the Alkali Lake isolates with those of bacteria from non-extreme environments suggested a common genetic origin of the 2,4-D degradation pathway in the two groups of micro-organisms.

2,4-Dichlorophenoxyacetic Acid↗

Microbial community analysis in the denitrification process of saline-wastewater by denaturing gradient gel electrophoresis of PCR-amplified 16S rDNA and the cultivation method.

The metallurgic wastewater generated from the processes of recovering precious metals from industrial wastes contains high concentrations of nitrogen compounds and salts. Biological nitrogen removal from this wastewater was attempted using a circulating bioreactor system equipped with an anaerobic packed bed or an anaerobic fluidized bed. The denitrification capability of the system with the anaerobic packed bed was more stable than that of the system with the anaerobic fluidized bed. The NOx removal rate of the anaerobic packed bed was as high as 97%. Microbial community analysis by denaturing gradient gel electrophoresis (DGGE) of PCR-amplified 16S ribosomal DNA (rDNA) fragments and the cultivation method revealed that the community diversity varied in accordance with wastewater composition such as the level of salinity and so on. Phylogenetic analysis suggested that the taxonomic affiliation of the dominant species in the anaerobic reactors was to the gamma-Proteobacteria including Halomonadaceae species. The PCR-DGGE method as a non-cultivation method was found to be a powerful tool for analysis of the microbial community, because the cultivation method could detect only a fraction of the microbial species present in these systems. The genetic diversity of the isolated bacteria belonging to the gamma-Proteobacteria which reduced both nitrate and nitrite in the anaerobic packed bed was higher than that of the bacteria in the anaerobic fluidized bed. This suggested that a genetically diverse microbial community stabilized the denitrifying performance in the anaerobic packed bed.

Journal Article↗

The diversity of culturable organotrophic bacteria from local solar salterns.

We isolated and cultured bacteria inhabiting solar saltern ponds in Taean-Gun, Chungnam Province, Korea. All of the isolated 64 strains were found to be moderately halophilic bacteria, growing in a salt range of 2-20 %, with an optimal concentration of 5% salt. Bacterial diversity among the isolated halophiles was evaluated via RFLP analyses of PCR-amplified 16S rDNAs, followed by phylogenetic analysis of the partial 16S rDNA sequences. The combination of restriction enzyme digestions with HaeIII, CfoI, MspI and RsaI generated 54 distinct patterns. A neighbor-joining tree of the partial 16S rDNA sequences resulted in the division of the 64 strains into 2 major groups, 45 strains of gamma-Proteobacteria (70.3%) and 19 strains of Firmicutes (29.7%). The alpha-Proteobacteria and Cytophaga-Flavobacterium-Bacterioides groups, which were repeatedly found to exist in thalassohaline environments, were not represented in our isolates. The gamma-Proteobacteria group consisted of several subgroups of the Vibrionaceae (37.5%), Pseudoalteromonadaceae (10.9%), Halomonadaceae (7.8%), Alteromonadaceae (7.8%), and Idiomarinaceae (6.3%). Members of Salinivibrio costicola (29.7%) were the most predominant species among all of the isolates, followed by Halobacillus treperi (12.5%). Additionally, three new species candidates were found, based on similarities of the 16S rDNA sequences to those of previously published species.

Bacillaceae↗

Major outer membrane proteins in moderately halophilic eubacteria of genera Chromohalobacter and Halomonas.

Outer and inner membrane fractions of Chromohalobacter marismortui and Halomonas elongata were isolated by differential detergent solubilization, and profiles of membrane proteins, especially major outer membrane proteins, were analyzed. These type strains possessed one extremely abundant outer membrane protein which showed similarity in amino-terminal amino acid sequence with the outer membrane porin proteins in other Gram-negative bacteria. Three halophilic eubacterial strains isolated from saline environments were also characterized. Strains 160 and 43 were found to be Chromohalobacter spp. and strain 40 to be a Halomonas sp. by sequence analysis of their 16 S ribosomal RNA genes. Extremely abundant porin proteins with an apparent molecular mass of 49 kDa were found in Chromohalobacter sp.160 and Halomonas sp. 40, but no major outer membrane protein was detected in Chromohalobacter sp. 43, suggesting strain 43 was most likely a naturally defective porin mutant. Porin proteins from Chromohalobacter spp. and Halomonas spp. showed the same migration on SDS-polyacrylamide gel electrophoresis with or without heat-treatment, indicating that these porin proteins did not form a SDS-resistant trimeric structure, which was detected in most of the Gram-negative bacterial porin proteins.

Amino Acid Sequence↗

Temperature and nutrient availability control growth rate and fatty acid composition of facultatively psychrophilic Cobetia marina strain L-2.

A facultative psychrophilic bacterium, strain L-2, that grows at 0 and 5 degrees C as minimum growth temperatures in complex and defined media, respectively, was isolated. On the basis of taxonomic studies, strain L-2 was identified as Cobetia marina. The adaptability of strain L-2 to cold temperature was higher than that of the type strain and of other reported strains of the same species. When the bacterium was grown at 5-15 degrees C in a defined medium, it produced a high amount of trans-unsaturated fatty acids. By contrast, in a complex medium in the same temperature range it produced a low amount of trans-unsaturated fatty acids. In the complex medium at 5 degrees C, the bacterium exhibited a three-fold higher growth rate than that obtained in the defined medium. Following a temperature shift from 11 to 5 degrees C, strain L-2 grew better in complex than in defined medium. Furthermore, when the growth temperature was shifted from 0 to 5 degrees C both the growth rate and the yield of strain L-2 growing in complex medium was markedly enhanced. These phenomena suggest that an upshift of the growth temperature had a positive effect on metabolism. The effects of adding complex medium components to the defined medium on bacterial growth rate and fatty acid composition at 5 degrees C were also studied. The addition of yeast extract followed by peptone was effective in promoting rapid growth, while glutamate addition was less effective, resulting in a cis-unsaturated fatty acid ratio similar to that of cells grown in the complex medium. These results suggest that the rapid growth of strain L-2 at low temperatures requires a high content of various amino acids rather than the presence of a high ratio of cis-unsaturated fatty acids in the cell membrane.

Cell Membrane↗