Square Haloarchaea of Walsby (SHOW)
(also known as "Square Bacteria" and "Haloquadratum walsbyi")

First described by Anthony Walsby in 1980, this organism managed to elude cultivation for 25 years until it was cultivated as part of my doctoral research. The first (mixed) culture was detected in the MDS lab in October 2002, with pure cultures being isolated by the following year. My work has been published in FEMS Microbiology letters - abstract. This paper was the second most downloaded FEMS Micro. Letters paper in the last quarter of 2004, and the most downloaded original research paper for that quarter!

My FEMS paper on the cultivation of the "square bacteria" is recommended by the Faculty of 1000 - you may see the evaluation here (you must have a subscription to the Faculty of 1000 - if you click the link from a university you should be able to go directly to the article).

Interest in this event was widespread, particularly internationally, with Nature.com carrying a news story (unfortunately now only available to Nature subscribers). Local interest included the Australian ABC (internet article only), while my institution, The University of Melbourne, carried an in-house story which may be seen here.

A second lab independently confirmed cultivation of the organism was possible, using quite different techniques, and published later in 2004 (Bolhuis et al, 2004). At present, work is being undertaken with that research group (Henk Bolhuis and others) to characterise this organism, tentatively named "Haloquadratum walsbyi", after its shape and initial discoverer.

Further information may also be found on Mike Dyall-Smith's website.

Haloarchaea - Why research them in Australia (and worldwide)?

Natural hypersaline environments are a significant part of Australia’s landscape and ecology, while artificial hypersaline lakes are being created to alleviate the country’s salinity problems and also for economic reasons, such as salt harvesting. The distinctive pink colouration of these lakes indicates that, far from being devoid of life, they in fact harbour large and active populations of microorganisms. Saline lakes are widely recognized as highly productive aquatic habitats, harbouring specialised assemblages of species and often supporting large populations of both migrating and breeding birds (Rodriguez-Valera, 1988). It is important to have an understanding of the microbial ecology of these environments, given the increasing importance of these environments in Australia, and also internationally - salt lakes make up about the same volume of the world’s bodies of water as freshwater systems. Of Australia’s largest five lakes, four are salt lakes - Lake Eyre (9500 km² when full), and the next two largest salt lakes in Australia, Lake Torrens and Lake Gardiner are 5745 and 4351 km² respectively (Geoscience, 2002).

The oceans are about 3.5% (w/v) salt, mainly NaCl, and contain the majority of halophilic microorganisms, including a wide variety of Bacteria and Eukarya (eg. protists and algae), and some Archaea. Extremely halophilic microrganisms grow between 15% salt up to saturation (around 37%), and previous studies have found that the dominant microorganisms in lakes with salinities approaching saturation are haloarchaea from the Family Halobacteriaceae (Benlloch et al., 2002), (Oren 2002). High salinity represents an extreme environment that relatively few organisms have been able to adapt to and occupy. While the diversity is low in these environments, the productivity and cell densities can be quite high. Even in lakes with saturated salt concentrations - when not dried out to salt pans, or after recent rains, salt lakes are usually near saturation, with a thick layer of crystalline salt as the lake bed - microbial cell densities can reach up to 107 to 108 cells per ml. These populations reflect a lack of predation and often quite high nutrient levels (Oren 2002).

The low total diversity in the lakes makes hypersaline lakes an ideal candidate system for ecological studies. Investigation into the nutrient cycling and population dynamics is a more manageable task than in a high diversity environment such as soil, which can contain as many as 12-18,000 species per gram (Torsvik et al., 1996). In particular, multi-pond solar salterns represent ideal candidate model systems due to their managed nature, in which salt concentrations are kept relatively constant over time, in contrast to natural systems which are more susceptible to climatic variation. Additionally, salterns exist around the world, albeit under somewhat different conditions. This provides a greater degree of international comparability than compared to natural systems.

Archaea are now widely considered the third Domain of life alongside Bacteria and Eukaryotes. Exhibiting features of both of the other Domains, Archaea represent a remarkable opportunity to study evolutionary relationships and the development of life. Archaea are also, in their own right, a diverse and significant part of the biosphere, particularly in “extreme” environments, although their distribution is otherwise as broad as Bacteria.

Haloarchaea, and particularly, the family Halobacteriaceae are members of the Domain Archaea, and comprise the majority of the prokaryotic population in hypersaline environments (Oren 2002). There are currently 15 recognised genera in the family (Gutierrez et al., 2002). The domain Bacteria can comprise up to 25% of the prokaryotic community, but is more commonly a much lower percentage of the overall population (Anton et al., 2000). At times, the alga Dunaliella salina can also proliferate in this environment (Casamayor et al., 2002).

Members of several genera within the Halobacteriaceae have been isolated from saltern crystalliser ponds, including Haloferax, Halogeometricum, Halococcus, Haloterrigena, Halorubrum, Haloarcula and Halobacterium families (Oren 2002). However, the viable counts in these studies have been small when compared to total counts, and the numerical significance of these isolates has been unclear. Only recently has it become possible to determine the identities and relative abundances of organisms in natural populations, typically using PCR-based strategies that target 16S small subunit ribosomal ribonucleic acid (16S rRNA) genes. While comparatively few studies of this type have been performed, results from these suggest that some of the most readily isolated and studied genera may not in fact be significant in the in-situ community. This is seen in cases such as the genus Haloarcula, which is estimated to make up less than 0.1% of the in situ community (Anton et al., 1999) but commonly appears in isolation studies.

Isolation of representative populations of the target environment offers significant potential both for the understanding of the ecological system and also for research into one of the most easily accessed Archaea, the Haloarchaea, but is limited by the lack of cultured representatives of the dominant species present in the environment as identified by Fluorescent In-Situ Hybridisation (Anton et al., 1999), clone library and microscopic analysis. At present many currently isolated representatives are thought to be only minor components of the total community (Anton et al., 1999).

However, isolation of pure strains is nevertheless an essential requirement to properly study organisms as it allows characterisation of their metabolic capabilities and hence an insight into their role in the natural environment. In addition, pure cultures allow investigations into the interaction of specific strains and/or other organisms in the home ecology.

As an example, pure strains are required for viral isolation to be undertaken. Viral populations are believed responsible for the majority of nutrient cycling and population turnover in hypersaline lakes through the lysis of infected cells. Bacterivory is absent in ponds above about 20% salinity, while viruses begin to be detectable at salinities above 15% (Pedros-Alio et al., 2000). Viral lysis is estimated to affect 7% of the total population per day, significant given the low doubling time of about 2 days for the in-situ prokaryotic population.

Viruses present a possible problem with isolation in liquid media due to the fact that viral loads are estimated at up to 10 times that of the prokaryotic population. Hence, an extinction culture containing only one cell may contain 10 times as many phage, some of which may have the potential to lyse the cell. This possibility is increased when the fact that the dominant organisms (and hence most likely to be at the end-point of the dilution series) are most likely to be the hosts for the largest phage populations.

The dominant organism, presumably responsible for a significant part of the nutrient cycling in the environment, is a square, flat and gas-vacuolated, bacteriorhodopsin containing archaeon first described by Walsby in 1980 (Walsby, 1980). After 25 years of attempts, it has recently been cultured as part of my doctorate (Burns et al, 2004; Bolhuis et al, 2004).

By combining molecular analytical methods with newer cultivation techniques, it may be possible to gain insight into the community structure and culture a greater percentage of the population such that most major groups are represented, as described by Burns et al, (2004b). In particular, it is imperative that the dominant microbial species present in a sample environment be isolated and characterised if any meaningful analysis of the natural ecology is to be made.

Cultivation of Haloarchaea

Please see here for an abstract of the paper describing this recent work. (pdf download available at the linked site)

Briefly, this work has demonstrated for the first time that it is possible to cultivate all numerically-significant organisms from a real environment - not just the ones that grow well in a laboratory. This has major implications for microbial ecology, as for the first time we can study both all of the organisms separately, as well as the interactions these organisms have with each other.
As the dominance of each organism in the lakes is known, this opens up the possibility of meaningful studies into the lake ecology to be undertaken using these organisms, rather than guessing at lake ecology using isolates which are not actually significant in the isolating environment – an extremely common situation in microbial ecology at present.

Haloarchaeal viruses - [this subsection courtesy Kate Porter, Dyall-Smith laboratory, The University of Melbourne]

[Further background information may also be found at my supervisor, Mike Dyall-Smith's, website here]

Viruses, which are dependant on their host cells for replication, must carefully regulate gene expression over the infection cycle.  As a result, viruses are frequently utilised to study fundamental aspects of gene expression and regulation.  In particular, the viruses of Archaea and Bacteria (bacteriophages) have proven to be extremely useful in the study of host genetics.  The first archaeal virus was discovered in 1974 (Torsvik and Dundas, 1974) and since this, around 39 archaeal viruses and virus-like particles (VLPs) have been reported (http://www.ncbi.nlm.nih.gov/ICTV/; Dyall-Smith et al., 2003; Häring et al., 2004), a miniscule number compared with over 5,100 bacteriophages (Ackermann, 2001; Ackermann, 2003).

Archaeal viruses are known to infect two of the four phylogenetic kingdoms (reviewed in Zillig et al., 1996; Ackermann, 2001; Ackermann, 2003).  The viruses of Crenarchaeota are morphologically diverse, belonging to at least five families: Fuselloviridae, “Globuloviridae”, “Guttaviridae”, Lipothrixviridae and Rudiviridae (http://www.ncbi.nlm.nih.gov/ICTV/; Arnold et al., 2000; Häring et al., 2004).  The viruses of Euryarchaeota are morphologically less diverse, with the majority belonging to the families Myoviridae and Siphoviridae, although one lemon-shaped virus and two lemon-shaped VLPs are known (http://www.ncbi.nlm.nih.gov/ICTV/; Bath and Dyall-Smith, 1998; Geslin et al., 2003a).  In addition, numerous VLPs of Crenarchaeota and Euryarchaeota, displaying diverse morphologies, have been observed in hot springs, hypersaline waters and deep-sea hydrothermal vents (Oren et al., 1997; Dyall-Smith et al., 2003; Geslin et al., 2003b; Prangishvili, 2003).  Although archaeal virus characterisation is still in its early stages, 19 genomes of archaeal viruses and VLPs have been completely sequenced:  13 species infecting Crenarchaeota and six infecting Euryarchaeota (http://www.ncbi.nlm.nih.gov/genomes/VIRUSES/viruses.html; Bath, 2004). 

   

The first haloarchaeal virus (halovirus) was observed in a preparation of crudely purified Hbt. salinarum flagella (Torsvik and Dundas, 1974).  Since this, 15 haloviruses have been isolated from numerous other sources (reviewed in Zillig et al., 1986; Zillig et al., 1988; Dyall-Smith et al., 2003).  Hypersaline waters are an especially good source of haloviruses and VLPs, as they contain high VLP concentrations.  In these environments, VLPs may outnumber cells by up to a factor of 9.5 (Oren et al., 1997).  The VLPs observed in such environments are of a variety of morphologies, including lemon-shaped, polyhedral and head-and-tail (Oren et al., 1997; Geslin et al., 2003b).  As hypersaline environments are, in general, devoid of protists that graze on prokaryotes, it seems probable that viruses are a major regulating factor of haloarchaeal populations. They may also play a significant role in mediating genetic transfer between cells.

Of the 15 halovirus isolates, most have head-and-tail morphologies and are monovalent, infecting Halobacterium species, although the more recent isolates infect members of the genera Haloarcula, Haloferax, Halorubrum and Natrialba.  All known haloviruses possess genomes of linear, double-stranded (ds) DNA and are capable of lytic multiplication within their hosts, although many haloviruses are able to enter lysogenic state or form persistent infection.  Halovirus particles are generally sensitive to low salt concentrations, although His1 and Hh1 can tolerate low salt media (Pauling, 1982; Bath and Dyall-Smith, 1998) and fN retains infectivity even in distilled water (Vogelsang-Wenke and Oesterhelt, 1988).  It appears that haloviral eclipse and latent periods and burst size may be regulated by the external salt concentration of the medium, a phenomenon that has been proposed to be significant for virus replication during changing salinity conditions in the environment (Daniels and Wais, 1990).

Relatively few haloviruses have been studied in detail at the molecular level.  The most thoroughly studied are fH, which has had extensive molecular characterisation (reviewed in Zillig et al., 1986; Zillig et al., 1988), and HF1, HF2, fCh1 and His1, whose complete genome sequences have been determined (http://www.ncbi.nlm.nih.gov/genomes/VIRUSES/viruses.html; Bath, 2004).  These five viruses have contributed greatly to archaeal genetics and have been utilised in transfection (Cline and Doolittle, 1987; Bath, 2004), gene cloning and expression (Blaseio and Pfeifer, 1990) and identification of restriction-modification systems (Pauling, 1982; Daniels and Wais, 1984; Patterson and Pauling, 1985).  The genome sequences have revealed interesting relationships among haloviruses and have demonstrated some links between archaeal viruses and bacteriophages.  fH and fCh1 display significant sequence similarity, surprising as the viruses are from considerably different environments and host ranges (Klein et al., 2002), whilst the HF1 and HF2 genome sequences are remarkably similar to one another, suggesting that the viruses only recently diverged and that the divergence was a single, major recombination event (Dyall-Smith et al., 2003; Tang et al., 2004).  The halovirus sequences also show varying degrees of resemblance to bacteriophages in genome organisation and replication strategy and in some cases there is significant gene sequence similarity.  This suggests that there has been horizontal transfer between the prokaryotic viruses, or that there was a common ancestor of viruses prior to the split between Archaea and Bacteria (Tang et al., 2002; Klein et al., 2002; Tang et al., 2004; Bath, 2004).

In addition to the haloviruses identified in the literature, this laboratory has isolated nine novel haloviruses from Australian hypersaline waters (Bath, 1995; Walker, 1999; Dyall-Smith et al., 2003).  Eight of these haloviruses were isolated in 1998 by plating hypersaline water samples directly on lawns of Haloarcula hispanica, Halorubrum coriense and Haloferax volcanii (Walker, 1999).  In initial studies, two of the viruses infecting Har. hispanica (designated PH1 and SH1) were revealed to possess a spherical morphology, which had previously been unobserved in euryarchaeal viruses (Walker, 1999; Seah, 2000; Porter, 2003).

Preliminary studies suggested that these two spherical viruses could be related to one another and possess an internal lipid membrane (Walker, 1999; Seah, 2000; Porter, 2003).  This virion architecture has been observed in many other viruses, including bacteriophages, such as PRD1 (Abrescia et al., 2004; Cockburn et al., 2004), eukaryotic viruses, such as adenovirus, and, recently, the archaeal virus STIV (Rice et al., 2004), suggesting a structural relationship between viruses from all three domains of life (Benson et al., 2004).  Several of these viruses also share a common replication system, which has only recently been observed in archaeal viruses (Bath, 2004).

References - General

Anton, J., Llobet-Brossa, E., Rodriguez-Valera, F., and Amann, R. (1999) Fluorescence in situ hybridization analysis of the prokaryotic community inhabiting crystallizer ponds. Environmental Microbiology 1: 517-523.

Benlloch, S., Lopez-Lopez, A., Casamayor, E.O., Ovreas, L., Goddard, V., Daae, F.L., Smerdon, G., Massana, R., Joint, I., Thingstad, F., Pedros-Alio, C., and Rodriguez-Valera, F. (2002) Prokaryotic genetic diversity throughout the salinity gradient of a coastal solar saltern. Environmental Microbiology 4: 349-360.

Bolhuis H., Poele E.M., Rodriguez-Valera F., (2004) Isolation and cultivation of Walsby's square archaeon. Environmental Microbiology Dec;6(12):1287-91.

Burns, D.G., Camakaris, H.M., Janssen, P.H. and Dyall-Smith, M. (2004a) Cultivation of Walsby’s square haloarchaeon. FEMS Microbiol. Lett. 238(2):469-473

Burns, D.G., Camakaris, H.M., Janssen, P.H. and Dyall-Smith, M. (2004b) Combined use of cultivation-dependent and cultivation-independent methods indicates that members of most haloarchaeal groups in an Australian crystalliser pond are cultivable. Appl. Environ. Microbiol. 70(9): 5258-5265.


Casamayor, E.O., Massana, R., Benlloch, S., Ovreas, L., Diez, B., Goddard, V.J., Gasol, J.M., Joint, I., Rodriguez-Valera, F., and Pedros-Alio, C. (2002) Changes in archaeal, bacterial and eukaryal assemblages along a salinity gradient by comparison of genetic fingerprinting methods in a multipond solar saltern. Environmental Microbiology 4: 338-348.

Connon, S.A., and Giovannoni, S.J. (2002) High-throughput methods for culturing microorganisms in very-low-nutrient media yield diverse new marine isolates. Applied and Environmental Microbiology 68: 3878-3885.

Geoscience Australia, http://www.auslig.gov.au/facts/landforms/larglake.htm#saltlake (2002).

Gutierrez, M.C., Kamekura, M., Holmes, M.L., Dyall-Smith, M.L., and Ventosa, A. (2002) Taxonomic characterisation of Haloferax sp. ("H. alicantei") strain Aa 2.2: description of Haloferax lucentensis sp. nov. Extremophiles Dec 2002;6(6):479-83.

Oren, A. (2002) Molecular ecology of extremely halophilic Archaea and Bacteria. FEMS Microbiology Ecology: 1-7.

Pedros-Alio, C., Calderon-Paz, J.I., MacLean, M.H., Medina, G., Marrase, C., Gasol, J.M., and Guixa-Boixereu, N. (2000) The microbial food web along salinity gradients. FEMS Microbiology Ecology: 143-155.

Torsvik, V., Sorhiem, R., and Goksoyr, J. (1996) Total bacterial diversity in soil and sediment communities - a review. Journal of Industrial Microbiology: 170-178.

Walsby, A.E. (1980) A square bacterium. Nature: 69-71.

References - Halovirus subsection

Abrescia, N. G. A., Cockburn, J. J. B., Grimes, J. M., Suton, G. C., Diprose, J. M., Butcher, S. J., Fuller, S. D., San Martin, C., Burnett, R. M., Stuart, D. I., Bamford, D. H. and Bamford, J. K. H. (2004).  Insights into assembly from structural analysis of bacteriophage PRD1.  Nature.  432, 68 – 74.

Ackermann, H.-W. (2001).  Frequency of morphological phage descriptions in the year 2000.  Archives of Virology.  146, 843 – 857.

Ackermann, H.-W. (2003).  Bacteriophage observations and evolution.  Research in Microbiology.  154, 245 – 251.

Arnold, H. P., Zillig, W., Ziese, U., Holz, I., Crosby, M., Utterback, T., Weidmann, J. F., Kristjansson, J. K., Klenk, H. P., Nelson, K. E. and Fraser, C. M. (2000).  A novel lipothrixvirus, SIFV, of the extremely thermophilic Crenarchaeon Sulfolobus.  Virology.  267, 252 – 266.

Bamford, D. H., Ravantti, J. J., Rönnholm, G, Laurinavi?ius, S., Kukkaro, P., Dyall-Smith, M., Somerharju, P., Kalkkinen, N. and Bamford, J. K. H. (unpublished).  Constituents of SH1, a novel membrane-containing virus infecting halophilic euryarchaeon Haloarcula hispanica.  Unpublished.

Bath, C. (1995).  Analysis of two novel bacteriophages of halophilic archaea (Bachelor of Science (Honours) thesis).  The University of Melbourne, Melbourne.

Bath, C. and Dyall-Smith, M. L. (1998).  His1, an archaeal virus of the Fuselloviridae family that infects Haloarcula hispanica.  Journal of Virology.  72, 9392 – 9395.

Bath, C. (2004).  The molecular biology of the halophilic archaeal viruses His1 and His2 (Doctor of Philosophy thesis).  The University of Melbourne, Melbourne.

Benson, S. D., Bamford, J. K. H., Bamford, D. H. and Burnett, R. M. (2004).  Does common architecture reveal a viral lineage spanning all three domains of life?  Molecular Cell.  16, 673 – 685.

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Cockburn, J. J. B., Abrescia, N. G. A., Grimes, J. M., Sutton, G. C., Diprose, J., Benevides, J. M., Thomas, G. J., Jr., Bamford, J. K. H., Bamford, D. H., Stuart. D. I. (2004).  Membrane structure and interactions with protein and DNA in bacteriphage PRD1.  Nature.  432, 12 – 125.

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Geslin, C., Le Romancer, M., Erauso, G., Gaillard, M., Perrot, G. and Prieur, D. (2003a).  PAV1, the first virus-like particle isolated from a hyperthermophilic euryarchaeote, “Pyrococcus abyssi”.  Journal of Bacteriology.  185, 3888 – 3894.

Geslin, C., Le Romancer, M., Gaillard, M., Erauso, G. and Prieur, D. (2003b).  Observation of virus-like particles in high temperature enrichment cultures from deep-sea hydrothermal vents.  Research in Microbiology.  154, 303 – 307.

Grant, W. D., Kamekura, M., McGenity, T. J. and Ventosa, A. (2001).  In Boone, D. R. and Castenholz, R. W (editors).  Bergey’s Manual of Systemic Bacteriology, Second Edition.  Volume One, The Archaea and the deeply branching and phototrophic Bacteria.  Springer-Verlag New York Incorporated, New York.

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