Genomes of Alteromonas australica,a world apart
© López-Pérez et al.; licensee BioMed Central Ltd. 2014
Received: 29 April 2014
Accepted: 13 June 2014
Published: 18 June 2014
Alteromonas is a genus of marine bacteria that is very easy to isolate and grow in the laboratory. There are genomes available of the species Alteromonas macleodii from different locations around the world and an Alteromonas sp. isolated from a sediment in Korea. We have analyzed the genomes of two strains classified by 16S rRNA (>99% similarity) as the recently described species Alteromonas australica, and isolated from opposite ends of the world; A. australica DE170 was isolated in the South Adriatic (Mediterranean) at 1000 m depth while A. australica H17T was isolated from a sea water sample collected in St Kilda Beach, Tasman Sea.
Although these two strains belong to a clearly different species from A. macleodii, the overall synteny is well preserved and the flexible genomic islands seem to code for equivalent functions and be located at similar positions. Actually the genomes of all the Alteromonas species known to date seem to preserve synteny quite well with the only exception of the sediment isolate SN2. Among the specific metabolic features found for the A. australica isolates there is the degradation of xylan and production of cellulose as extracellular polymeric substance by DE170 or the potential ethanol/methanol degradation by H17T.
The genomes of the two A. australica isolates are not more different than those of strains of A. macleodii isolated from the same sample. Actually the recruitment from metagenomes indicates that all the available genomes are found in most tropical-temperate marine samples analyzed and that they live in consortia of several species and multiple clones within each. Overall the hydrolytic activities of the Alteromonas genus as a whole are impressive and fit with its known capabilities to exploit sudden inputs of organic matter in their environment.
KeywordsAlteromonas australica Biogeography Alteromonas Genomic Island Population genomics Integron
The genus Alteromonas contains species of marine bacteria that have been isolated often from the oceans around the world [1, 2]. The type species Alteromonas macleodii is found worldwide but mostly at temperate or tropical latitudes due to its mesophilic nature (grows between 10 and 45°C) (López-Pérez and Rodriguez-Valera, in press). This microbe was shown to be enriched in the particulate fraction of the water column in off-shore Mediterranean waters [3, 4]. In the Mediterranean Sea, bacteria of this species can be found even at high depths due to the relatively warm temperatures of its deep water mass (ca. 13°C) . Related microbes have been found to bloom in mesocosms in the central Pacific gyre when the water was enriched with natural seawater nutrients [6, 7]. Other species of Alteromonas (e.g., A. stellipolaris) have been isolated from polar environments (Antarctic sea water) and are more psychrophilic .
Previously the genomes of two A. macleodii strains, AltDE and AltDE1 isolated from the South Adriatic at 1000 m depth were analyzed . The average nucleotide identity (ANI) over the core genome between the two strains was 98.5%. From the same sample several other strains were isolated. The characterization by PCR amplification of their 16S rRNA gene classified one of them as belonging (99% identity) to the recently described species Alteromonas australica . This bacterium (strain H17T) was collected from the first meters below the surface at St. Kilda beach, in Port Phillip Bay (Tasman Sea, Pacific Ocean). When comparing AltDE and AltDE1  in spite of their high similarity, their genomes differ markedly in their content of flexible genomic regions or islands. These can be classified into two main types . One type is typically associated to mobile genetic elements (including lysogenic phages). They tend to be found at the same genomic location and context but they are often completely absent from some strains. They have been designated "additive genomic islands"  because they typically vary by the presence/absence of gene cassettes in some strains but not in others. They carry lifestyle related genes, that include different metabolic properties (for example the degradation of organic compounds such as urea) or biotechnologically relevant features such as the polysaccharide or the polyketide synthase (PKS) clusters . The second type are the "replacement genomic islands", in which completely different gene clusters with similar assigned functions are found at the same genomic location. They are typically involved in structural features of the cells exposed to the environment. Recent evidence indicates that they are exchanged by homologous recombination . The gene cluster coding for the genes of the O-chain (sometimes called O-antigen) of the Gram negative lipopolysaccharide being a paradigmatic example.
This study aimed to provide a detailed genomic analysis of the two A. australica strains. We have fully sequenced and assembled these two genomes and compared them with all the available genomes of strains within the genus Alteromonas. The patterns of variation observed between the two A. australica strains are very similar to the ones found before when comparing the isolates from the same location mentioned above [9, 11]. Across the genus, the location and functional nature of the genomic islands was preserved, although obviously the genetic content was very different. However, some remarkable examples of conservation were found in the additive genomic islands with the members of A. macleodii.
General features of genomes
A. australica H17T
A. australica DE170
A. macleodii DE
A. macleodii ATCC 27126T
Alteromonas sp. ALT199
Alteromonas sp. SN2
GC content (%)
Tasman Sea (Australia)
Pacific Ocean (Hawaii)
Pacific Ocean (San Diego)
Yellow Sea (South Korea)
Depth of Sample (m)
In order to analyzed the impact of the homologuos recombination in the evolution of the core genome of the members of the Alteromonas genomes we used ClonalFrame software v1.2  to estimate two different values, r/m and ρ/θ. The parameter r/m shows the weight of recombination in the diversification of the species relative to mutation, whereas ρ/θ measures the absolute number of events of recombination relative to mutation. The results showed that within the Alteromonas genus the 95% credibility interval of ρ/θ was 0.01-0.02 (mean = 0.01), indicating that recombination happened hundred times less frequently than mutation. However, the impact of recombination had a predicted significant effect in the evolutionary process as showed by the r/m value of, 0.60 (with 95% credibility interval 0.45-0.91), suggesting that recombination introduces several polymorphisms per event. The average size of the fragments affected by recombination was 1102 bp (with a 95% credibility interval of 799 to 1349 bp), similar to those found in other bacteria, such as Bacillus cereus  and Chlamydia psittaci . In a previous study carried out with the nine genomes belonging to the A. macleodii deep ecotype  we obtained similar results for the comparison of all the A. macleodii members (deep and surface ecotype) with values of r/m = 0.45 and ρ/θ = 0.06. However, when only the deep ecotype members were considered, both parameters were higher, ρ/θ (0.58) and r/m (5.13), suggesting that recombination is an important factor in the evolution within this clade. Using the locally collinear blocks generated from the whole-genome alignments we have also analyzed the existence of recombination events by building ML trees of randomly selected regions (Additional file 1: Figure S2). The results show frequent variations of the topology suggesting recombination events taking place across the Alteromonas genus, but only in small fragments of less than 3 Kb. However, topology was stable when fragments of more than 5 Kb were selected.
Flexible genomic islands
Characteristics of genomic islands found in A. australica H17 T and DE170 genomes
Flexible genomic islands
O-chain of LPS
Strain specific genomic islands
Type I RM system
Type I RM system
Cellulose synthase cluster
fGI1 is of the additive kind and is a typical example of genomic island in which a conserved tRNA act as an insertion target for gene cassetes . Addittion of different cassettes makes the length variable among the strains, going from more than 110 Kb in A. macleodii DE (AltDE) and A. australica DE170 to a single cassette in A. macleodii ATCC 27126T (Additional file 1: Figure S3). Two different kinds of cassettes were found, one is composed of different clusters of czcABC genes, encoding the components of heavy metal efflux pumps important for resistance to cobalt, zinc and cadmium. The other contains a complete hydrogenase cluster. It is remarkable that this hydrogenase cluster previously described in the strain AltDE  from the Adriatic Sea, has been also found with a similarity higher than 99% in the Tasman Sea isolate H17T (Additional file 1: Figure S3). However, it is not present in A. australica strain DE170 that comes from the same water sample than AltDE. This cluster is also present in all the members of the A. macleodii deep clade, with the single exception of the strain A. macleodii 615 isolated from the English Channel. The AltDE cluster has been expressed as an active enzyme in both E. coli  and in the cyanobacterium S. elongates . A similar (87% nucleotide identity) hydrogenase cluster was found in a Glaciecola sp. 4H-3-7 + YE-5 (an isolate from marine subseafloor sediments Suruga Bay, Japan) plasmid .
Strain specific genomic islands
In addition, there are genomic islands that are found only in one of the strains. Five unique islands were found in strain H17T and six in strain DE170 (Table 2). H17T GI5 contains a gene cluster encoding a methanol/ethanol pyrroloquinoline quinone (PQQ)-dependent dehydrogenase and the putative pqqABCDEF operon that is used as a cofactor and have also shown to be an important antioxidant agent against oxidative damage . This GI was located next to a single Leu-tRNA and at the end of this GI we found a direct repeat identical to the last 52 nucleotides of the tRNA 3′ end, evidence that the tRNA has acted as an insertion target of the GI in the same way as we found in fGI1. Methanol/ethanol dehydrogenase is a key enzyme used for growth in the presence of methanol/ethanol . However, the growth on a one carbon substrate requires a complex metabolic machinery that has not been detected in Alteromonas yet. In fact, phenotypic analyses reveal that none of the two strains are able to grow in minimal medium with 1% of methanol (or ethanol) as sole carbon and energy source.
Some of the GIs appear to be associated to post-segregation killing systems. These systems have been mainly described as defense mechanisms against foreign DNA and involved in the stabilization of mobile elements . GI2 in both strains encoded for a different classic type I restriction modification systems. Along the same lines, in the strain H17T GI1 a complete gene cluster for a DNA backbone S-modification (phosphorothioation) was identified . This system seems to act similarly to the classical restriction systems type I but protects DNA using phosphorothioation instead of methylation. The H17T cluster is composed by seven genes, dndBCDE that are required for the DNA S-modification and another set (dptFGH) involved in the restriction of the unmodified DNA . A. australica DE170 genome contains a mobilizable genomic island (MGI) (GI11). MGIs have been recently described as conjugative mobile elements that utilize the conjugation machinery of Integrative Conjugative Elements (ICE) or plasmids for their transfer. This GI could be considering other kind of "additive islands" . In a recent study, five putative MGIs have been characterized in several strains of A. macleodii  sharing the same insertion point with the one of DE170.
Most of the heavy metal resistance genes in Alteromonas are clusterd in fGI1. In addition, strain DE170 have another GI containing a large cluster of genes that code for metal resistance related proteins. This 36 Kb region that was flanked by transposases was nearly identical to a region in the plasmid from Glaciecola sp. strain 4H-3-7 + YE-5 (pGLAAG01, 341 Kb). Interestingly, this plasmid was showed to be highly syntenic with the plasmid pAMDE1-300 from A. macleodii DE1 isolated from the same location as strain DE170 . However, both plasmids have a large variable region with very different genes. Within the variable part in pGLAAG01 was this metal resistant GI found within the chromosome of strain DE170. In the case of pAMADE1-300 the variable region contains a hybrid NRPS-PKS cluster of 65 Kb  that was also found within the chromosome of two other A. macleodii strains . These results illustrate the plasticity of these genomic elements that appear to cross easily the genus barrier.
GI4 and GI5 of DE170 appear to be involved in xylan degradation and cellulose biosynthesis. Xylan, a complex polysaccharide with a β-1,4-linked backbone of xylose, is the second most abundant plant cell wall polysaccharide . The xynTAB and xylREAB clusters that code for the enzymes involved in the degradation and its conversion to D-xylulose 5-P, a pentose phosphate pathway intermediate, were all found in GI4 of DE170. Phenotypic analysis showed that strain D170 was indeed able to grow using xylan as a unique carbon and energy source while strain H17T was not (see Methods). Also in DE170, the complete operon for bacterial cellulose synthesis (bcs) was found in GI10. This operon contains the genes that code for the two catalytic subunits, BcsA and BcsB, that are a transmembrane complex involved in the synthesis of cellulose from glucose and its and secretion. The other components (BscC and BscZ), are accessory proteins related to the regulation and the assembly of the complex . Bacteria generally produce cellulose as a component of the extracellular matrix involved in biofilm formation and cell adhesion .
Both A. australica strains contain a genomic region with high similarity to CP4–57, a putative defective prophage described in Escherichia coli . This prophage participates actively in E. coli biofilm development . Like its E. coli counterpart, this putative prophage was found in both H17T and DE170 genomes inserted at one tRNA (Leu) gene that contains a similar att site to the one described for prophage CP4-57 [51, 52]. A similar putative prophage was found at the equivalent location in three highly similar isolates of A. macleodii "deep ecotype" belonging to the same clonal frame and obtained from a deep sample (~3500 m) from the Urania Basin in the Ionian (Mediterranean) . Actually, widely divergent versions of this prophage have been found in most Alteromonas genomes available, including the widely divergent SN2 (Additional file 1: Figure S7). In the A. australica strains the versions of this putative prophage were very divergent in sequence. The H17T version was much more similar to the Urania isolates and the DE170 strain version was more similar to the isolate from the Yellow Sea sediment SN2 (Additional file 1: Figure S7).
Recruitment from metagenomes
We have compared the recruitment of the genomes in different published marine metagenomes in order to compare the relative abundance of different species [18, 55]. These include both central North Pacific and North Atlantic gyres (Hawaii Ocean Time Series-HOTS and Bermuda Atlantic Time Series-BATS) metagenomes [56, 57] and the different collections of the Global Ocean Survey (GOS)  among others (see Methods). A restrictive cut-off of 98% of identity in 90% of the length of the environmental read was established to perform BLASTN comparisons against the genome of a representative of each species of Alteromonas. Unfortunately with the single exception of the deepest Mediterranean basin Matapan-Varilov  none of the Alteromonas genomes recruit significantly from marine metagenomic datasets (Additional file 1: Figure S9). From the Matapan-Varilov sample the A. australica genomes recruit similarly to A. macleodii DE, indicating a possible large particle habitat  also for this species. We also compared the genomes with the Dissolved Organic Matter (DOM), Deep Sea Water (DSW) and Dauphin Island Cubitainer Experiment (DICE) metatranscriptomes [6, 7, 60]. These three microcosms experiments were designed to analyze the transcriptional response of the bacterial community from ocean surface waters to adding dissolved organic matter (DOM and DICE) and deep seawater samples (DSW). Interestingly, all the species representative genomes (one for each since the method cannot distinguish differential recruitment within a single species, see Methods) recruit highly in these metatranscriptomes (Additional file 1: Figure S9).
The two genomes described here are the first from a species of Alteromonas formally described as different from A. macleodii. Actually the genome of strain SN2 also belongs to what certainly is a separate species, although it has not been formally described as such and remains as Alteromonas sp. We have also the added advantage that the two available genomes come from isolates obtained in very different locations (actually from nearly exact geographic antipodes) and habitats (surface coastal waters versus bathypelagic and off-shore). The first fact to underline is the remarkable similarity between the two genomes that actually recalls the diversity found for A. macleodii concurrent isolates. This supports the global distribution of Alteromonas species compounded with a high diversity of concurrent clones at every specific location. We posit that Alteromonas populations and actually most, if not all, prokaryotes live in complex consortia of multiple clones that have different gene complements, increasing the activities and environmental ranges in which the population can be successful [61, 62].
The core genome of all the strains of Alteromonas described to date (ca. 2000 genes) is relatively large (see below) although the ANI found among these microbes (Figure 2) indicates that they are widely divergent lineages as expected from strains from different species within the same genus. The core genome could shrink as new strains are sequenced. Particularly the species that live in cold environments such as A. stellipolaris isolated from Antarctic sea water , might have quite different gene pools reflecting their different habitats. As a reference, in the comparison of 7 species of the genus Pseudomonas which genome has a similar genome size to the genus Alteromonas, were found ca.1500 genes making up the core . In the same way, 11 species of the genus Glaciecola that belong to the same family had 1257 genes . Actually, from the ANI values A. macleodii could be in really composed of at least 3 species, the strains defined as the deep ecotype, the yellow sea isolate and the global surface ecotype with ANIs ranging from 73.7 to 80.6%. With this proviso we would be dealing with the equivalent of 5 different species genomes in this calculation of the Alteromonas core genome. The flexible part of the genome thus far would add up to ca. 13000 genes, also a typical value if is compared with the marine bacteria of the related genus Glaciecola (17276 gene families)  or the more than 17000 of the Vibrio pangenome .
A remarkable phenomenon that we have discovered is the continuum at the level of the genes found in the flexible genome across the genus. The fact that flexible genomic islands are found at equivalent genomic context, even when considering different species of the same genus, indicates that they are quite stable genomic features. In addition, we found remarkable examples of conservation in the flexible genome. For example, the presence of a nearly identical hydrogenase cluster shared by A. macleodii DE (Mediterranean Sea) and H17T (Tasman Sea), or the presence of nearly identical integron cassettes in the two A. australica strains. This was expected from the mobile nature of these genetic elements. However, the absolute lack of geographic patterns was more unexpected . Also, the conservation of these elements is nearly perfect, indicating that they have been exchanged recently, in spite of the large geographic distance. Some fGIs that are not mobile such as the flagellum glycosylation have also been found to be perfectly conserved in strains of distant geographic origins . It seems that the core genome diverges more (at the level of SNPs) than the flexible one, probably because the latter is much more homogenized due to its frequent exchange, either by homologous or illegitimate recombination. In addition, flexible genes jump over the species barriers much more often than the core genome.
The recruitment, mostly from metatranscriptomes indicates that i) the genus Alteromonas is one of the most actively blooming microbes in sea water, ii) they have a worldwide distribution from the deep waters of the Mediterranean to the Pacific and Atlantic oceans and iii) they appear in complex consortia of multiple species. It was already known that A. macleodii lives in complex consortia of multiple clonal lineages that appear concurrently at any given sample . A similar situation has been found for other marine microbes such as Prochlorococcus . It would seem that the same applies to different species within the same genus. This adds to the plankton paradox  including even more diversity levels to the populations within the same communities.
The two genomes of A. australica described here have a similar pattern of variation than the two isolates of A. macleodii isolated from the same location in the deep Mediterranean and previously described. Although the genomes are largely syntenic and with a high ANI over the homologous regions, large flexible genomic islands are markedly different in the two strains. This fGIs are of two types, i) the total replacement fGIs, in which the gene cluster in one strain is completely different in gene content from the other strain but with similar assigned function, and ii) the additive fGIs in which gene cassettes are added or deleted depending on the strains but retain some similar regions. It is remarkable that in spite of the large difference in ANI between A. australica and A. macleodii the fGIs are located at equivalent positions and with similar assigned functions (at least for the replacement type).
Like in the case of A. macleodii, metagenomic recruitments indicate that the different strains coexist at the same locations and have probably a global distribution in temperate and tropical latitudes. Both A. macleodii and A. australica are bloomers that increase their presence in fertilized mesocosms when an input of nutrients is provided.
Sample collection and sequencing
Details of isolation and origin of the Alteromonas strains using in this study have been described in Additional file 1: Figure S1. DNA was extracted by phenol-chloroform as described in  and checked for quality on a 1% agarose gel. The quantity was measured using Quant-iT® PicoGreen® dsDNA Reagent (Invitrogen). The genomes were sequenced using the IlluminaHiSeq 2000 (100-bp paired-end read) sequencing platform (Macrogen, Korea). The generated reads were trimmed and assembled de novo with VELVET, version 0.7.63  using default parameters except for the k-mer that was 49. Combination of Geneious Pro 5.0.1 (with default parameters) using previously Alteromonas assembled genomes as a reference [9, 11, 18] and oligonucleotides designed from the sequence of the ends of assembled contigs were used in order to obtain one single closed contig.
Genome annotation and analysis
The genomes were annotated using the NCBI PGAAP annotation pipeline (http://www.ncbi.nlm.nih.gov/genome/annotation_prok/). The predicted protein sequences were compared using BLASTP to the NCBI nr protein database (e-value 10-5). ORFs smaller than 100 bp and without significant homology to other proteins were not considered. BioEdit was used to manipulate the sequences . GC content was calculated using the EMBOSS tool geecee . For comparative analyses, reciprocal BLASTN and TBLASTXs searches between the genomes were carried out, leading to the identification of regions of similarity, insertions and rearrangements. To allow the interactive visualization of genomic fragment comparisons Artemis v.12 , Artemis Comparison Tool ACTv.9  were used to compare the genomes. The ANI between strains was calculated using JSpecies software package v1.2.1 using default parameters . Sequences were aligned using MUSCLE version 3.6  and ClustalW  and edited manually as necessary. Nucmer program in the MUMmer3+ package  was used to identify the indels and the SNPs between small regions of the genomes. Pan Genome Analysis Pipeline (PGAP)  was used to identify all of the orthologous pairs genes between Alteromonas genomes. The common dataset of shared genes among the strains was defined as their core genome. The total set of genes within the genomes was defined as the pan genome. The set of genes in each strain not shared with other strains was defined as unique genes.
To determine the exact phylogenetic relationship of the new isolates within the genus, phylogenetic analysis for all the Alteromonas members whose genomes were available were carried out (Additional file 1: Table S1). The tree was rooted using Pseudoalteromonas atlantica T6c (NC_008228.1) as an outgroup. The complete genomes were analyzed using TIGRfams to identify and concatenated all the conserved proteins. The concatenated proteins were aligned using Kalign  and a maximum likelihood tree was made using FastTree  using a JTT + CAT model and a gamma approximation.
The first step to analyze the recombination events among the Alteromonas strains was to make a multiple genome alignment. This was performed by using Mauve multiple alignment software (v2.3.1) . ClonalFrame software v1.2 , a Bayesian inference method that reconstructs clonal relationships between the isolates in a sample, was used for estimating mutation and recombination rates. Three independent runs of ClonalFrame were performed each consisting of 100000 Markov chain Monte Carlo iterations. To assess the relative contribution of recombination and mutation, r/m and ρ/θ statistics were used.
Recruitments of environmental collections
Genomes recruitments were carried out against some available marine metagenomes and metatranscriptomes [BATs (Bermuda Atlantic Time Series) , DICE (Dauphin Island Cubitainer Experiment) , DOM (Dissolved Organic Matter) , DSW (Deep Sea Water) , GOS (Global Ocean Survey) , HOTs (Hawaii Ocean Time Series) [57, 82], Marmara , MedDCM (Mediterranean Deep Chlorophyll Maximum)  and MVP (Matapan-Vavilov Deep) ]. BLASTN was carried out between the genome of a representative member of each Alteromonas species (A. australica DE170; A. macleodii ATCC27126T; A. macleodii DE; Alteromonas sp. ALT199 and Alteromonas sp. SN2) and the environmental databases. A restrictive cut-off of 98% of identity in 90% of the length of the environmental read was established to guarantee that only similarities at the species level were counted. The number of hits was normalized against the genomes and the database sizes.
Growth assays in media with xylan as a sole a carbon and energy source were carried out in order to study if the presences of this gene cluster provided extra abilities in strain DE170. A 50 ml culture of both A. australica strains were grown in marine broth at 20°C until they reached to late exponential growth phase (Optical density 600 nm = 1.0). The cultures were washed twice using minimal medium without any carbon sources and then grown in minimal medium agar plates supplemented with 0.5, 1, 5 and 10 g l-1 of xylan from beechwood (Sigma; ×4252) at 20°C. The same washed cultures were used to analyze the Methanol/Ethanol dehydrogenase activity. To measure growth rate, cultures were grown in minimal medium with 1% ethanol or methanol as a sole carbon source in Erlenmeyer flasks with orbital shaking (200 rpm) and incubated at 20°C. Growth was measured by the optical density at 600 nm.
The genome sequences have been deposited in GenBank under the following bioproject accession numbers; PRJNA246143 for A. australica H17T and PRJNA246140 for A. australica DE170.
This work was supported by projects MICROGEN (Programa CONSOLIDER-INGENIO 2010 CDS2009-00006), CGL2009-12651-C02-01 from the Spanish Ministerio de Ciencia e Innovación, DIMEGEN (PROMETEO/2010/089) and ACOMP/2009/155 from the Generalitat Valenciana and MaCuMBA Project 311975 of the European Commission FP7. FEDER funds supported this project.
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