Comparative analyses of actinobacterial genomic
fragments from Lake Kinneret
Alon Philosof, Gazalah Sabehi and Oded Béjà*
Faculty of Biology, Technion – Israel Institute of
Technology, Haifa 32000, Israel.
Summary
The high genomic G+C group of Actinobacteria pos-
sesses a variety of physiological and metabolic prop-
erties, and exhibits diverse lifestyles and ecological
distribution. In recent years, Actinobacteria have been
found to frequently dominate samples obtained from
freshwater samples. Furthermore, phylogenetic analy-
ses have shown that 16S rRNA genes from uncultured
actinobacterial freshwater samples cluster in four dis-
tinct lineages. While these lineages are abundant, little
is known about them and currently no pure-culture
representatives or genomic fragments of them are
available. In a screen of a genomic library from the
moderately eutrophic freshwater Lake Kinneret, five
fosmid clones containing actinobacterial genomic
fragments were found. Three ~40 kb genomic frag-
ments were chosen for sequencing. Fosmids K003 and
K005 showed high similarity and were affiliated with
the acIV actinobacterial freshwater lineage. Fosmid
K004 was affiliated with the highly abundant acI
lineage. A comparative genomic analysis revealed
high synteny between the two freshwater clones K003
and K005 but a lower synteny between these two and
the K004 fosmid. Fosmids K003 and K005 share an
identical arrangement of arginine biosynthesis gene
while K004 showed a slightly different arrangement by
lacking the argF gene. Fosmid Ant4E12, an Antarctic
actinobacterial clone, showed a higher synteny with
K003/5 than K004 and a similar arginine operon, but in
a different genomic context. The Clusters of Ortholo-
gous Groups categories assignment of the three
fosmids yielded genes that were mostly involved in
amino acid and nucleotide metabolism, as well as
transport and ribosomal RNA translation, structure
and biogenesis. These genomic fragments represent
the first sequences to be published from these lin-
eages, providing a cornerstone for future work on this
environmentally dominant group.
Introduction
Actinobacteria, a high G+C content Gram-positive
phylum, ranging between 51% in some corynebacteria
and more than 70% in Streptomyces and Frankia
(Ventura et al., 2007), are abundant in diverse environ-
ments, including extreme habitats, soil, marine and fresh-
water (Glöckner et al., 2000; Rondon et al., 2000; Zwart
et al., 2002; Cottrell et al., 2005; Ward and Bora, 2006).
This phylum possesses a wide variety of physiological
and metabolic properties, such as the production of extra-
cellular enzymes and a variety of secondary metabolites,
including many potent antibiotics (Goodfellow and Will-
iams, 1983; Ward and Bora, 2006; Ventura et al., 2007).
Furthermore, members of the Actinobacteria phylum
exhibit diverse lifestyles, including pathogens, nitrogen-
fixing symbionts, plant commensals, gastrointestinal tract
inhabitants and more (Ventura et al., 2007).
Actinobacteria are common in a variety of freshwater
habitats and are distributed globally (Hiorns et al., 1997;
Zwart et al., 2002; Sekar et al., 2003; Warnecke et al.,
2005). In addition, Actinobacteria comprise the majority of
bacterioplankton in many freshwater habitats (Glöckner
et al., 2000; Hahn et al., 2003; Allgaier and Grossart,
2006). Phylogenetic analyses based on partial and nearly
complete 16S rRNA gene sequences revealed distinct
phylogenetic lineages of freshwater Actinobacteria (Zwart
et al., 2002; Warnecke et al., 2004). The four lineages,
acI-IV (Warnecke et al., 2004), appear to be diverse, con-
taining sequences originating from different habitats such
as rivers, lakes and estuaries (Warnecke et al., 2004;
Allgaier and Grossart, 2006). Lineage acI, probably the
most abundant of the four, is distributed globally in highly
diverse environments and currently has no isolates in
culture (Warnecke et al., 2004; 2005; Lindström et al.,
2005; Allgaier and Grossart, 2006; Allgaier et al., 2007;
Newton et al., 2007). This lineage is divided into sub-
clusters, which appear to relate to ecophysiological
differences (Newton et al., 2007). The acII lineage,
also globally distributed, contains several ultramicrobial
isolates in two of its subclusters (acII-B and acII-D)
(Ludemann and Conrad, 2000; Hahn et al., 2003;
Warnecke et al., 2004; Hahn and Pockl, 2005). Current
sequences of the acIII lineage were obtained from hyper-
saline, humic and soda lakes. (Humayoun et al., 2003;
Warnecke et al., 2004; Newton et al., 2006; Wu et al.,
Received 25 November, 2008; accepted 26 June, 2009. *For corre-
spondence. E-mail beja@tx.technion.ac.il; Tel. (+972) 4829 3961;
Fax (+972) 4822 5153.
Environmental Microbiology (2009) 11(12), 3189–3200 doi:10.1111/j.1462-2920.2009.02024.x
© 2009 Society for Applied Microbiology and Blackwell Publishing Ltd