Australian freshwater cyanobacteria: habitats and diversity
Glenn B. McGregor
Environment and Resource Sciences
Queensland Department of Environment and Resource Management
120 Meiers Road, Indooroopilly Qld 4068, Australia
glenn.mcgregor@derm.qld.gov.au
2
Introduction
The cyanobacteria are a morphologically diverse group of prokaryotes, known to
occur in almost all biotopes including lakes, rivers and streams, man made ponds, and
reservoirs (Mur et al. 1999), oceans and estuaries (Hoffmann 1999), and extreme
environments such as thermal springs (Weller et al. 1991, Ferris & Ward 1997, Ward
et al. 1998), hypersaline microbial mats (Garcia-Pichel et al. 1998, Nübel et al. 2000),
desert soils (Garcia-Pichel et al. 2001) and Antarctic lakes (Taton et al. 2003, 2006).
It is partly due to their versatile metabolism and their ability to rapidly switch from
one mode to another, that they are successful in such a wide range of environments
(Stal 1991). As such, they provide a significant contribution to the primary
productivity of most aquatic ecosystems and indeed the biosphere (Stockner & Antia
1986, Pace 1997). Many species produce secondary metabolites that are either toxic
or impart unpleasant taste and odour to the water and as such are well known to the
water industry (Chorus & Bartram 1999).
“Nuisance” cyanobacteria came to the Australian national attention in the summer of
1991 when a bloom of the potentially toxic species Anabaena circinalis affected a
1000 km stretch of the Murray River (Davis 1997). During 1991 every mainland state
of Australia had to deal with cyanobacterial blooms; reservoirs were closed and
emergency drinking water was trucked in for town drinking water. These blooms
were significant as they focussed the combined efforts of the water industry and
Federal and State agencies and led to the provision of resources to support critical
research into the prevention and management of cyanobacterial blooms in the
Australian context. In the preceding years a significant body of scientific knowledge
had been generated around this issue as it relates to the water industry; however this
research did not address the fundamental lack of basic knowledge of cyanobacterial
(and microalgal) diversity across the range of habitats represented on the Australian
continent.
Despite their importance, there are very few comprehensive regional accounts of
cyanobacteria biodiversity in the scientific literature. Indeed the cyanobacterial
microflora of Australia is poorly known, particularly from the tropical regions and
niches including benthic and extreme environments. The first references of
cyanobacteria from Queensland date from Bailey (1893, 1895, 1898) and while a
number of works have documented them as part of more general microalgal floral
studies of north-eastern Australia (e.g. McLeod 1975, Ling & Tyler 1986, 2000) or
restricted studies of specific groups since then (e.g. Baker 1991, 1992, Baker &
Fabbro 1999, McGregor & Fabbro 2001, McGregor et al. 2007), there still remains no
comprehensive study with a specific focus on Australia’s freshwater cyanobacteria.
Recent studies have shown that the diversity of cyanobacteria from tropical regions is
considerably larger than is apparent from the literature (Komárek 1985a, 1985b,
Komárek & Kaštovský 2003). It is clear that new data on cyanobacteria from
different natural habitats across Australia’s tropical and sub-tropical regions are
urgently required to gain a better understanding of cyanobacteria diversity.
Information on the diversity of Australian cyanobacteria is also required from a
conservation perspective. A major impediment to implementing conservation
strategies for Australia’s freshwater cyanobacteria and algal biodiversity is the lack of
distributional data for most species, and a lack of understanding of the “taxonomic
uniqueness” of previously reported taxa (Scott et al. 1997, ACIL 2002). This is
3
largely due to a paucity of detailed floristic studies and a complete absence of a
thorough Australian algal treatise. While comprehensive systematics are essential to
fully assess endemism, rarity, and “weediness”, and to reveal phylogenies and
biogeographic patterns, the delineation and nomenclature of Australian species is of
immediate concern (Skinner & Entwisle 2001). Floristic documentation of this kind
is required for the adequate conservation, management and appreciation of Australian
freshwater algae, including the cyanobacteria within a broader global context. This
review provides some examples of Australian freshwater cyanobacterial diversity and
how it relates to specific habitats based on our current but limited understanding.
Lakes and reservoirs
Blooms of cyanobacteria represent one of the most conspicuous waterborne microbial
hazards to human and agricultural water supplies, fisheries production and freshwater
and marine ecosystems. This hazard results from the production of harmful
cyanotoxins by multiple species, along with BOD and surface water deoxygenation
issues associated with seasonally high biomass of micro- and macroalgae and
cyanobacteria. This can manifest itself within reservoirs and in downstream receiving
water systems during releases, and in estuaries and shallow coastal bays. As the
demand on limited water resources grows against a backdrop of increasing climate
variability there is an urgent need to quantify water quality security risks. This
information is vital for assessing the human and ecological impacts of future water
resource management including inter-basin transfers and recycled water reuse, and to
support the development of regional water supply strategies.
Surface water contributes approximately 96% of the distributed water supplied by the
Australian water supply industry (ABRS 2006). A significant proportion of this
supply is dependent on large surface water storages. Man-made water storages
(reservoirs and weir pools) are the most common, permanent lentic habitats
throughout north-eastern Australia. Reservoirs are generally larger than weir pools,
are not confined within the original river or stream channel, are characterised by high
pH, mean summer surface water temperature between 28°C and 32°C, a highly stable,
thermally stratified water column, long hydraulic retention time (> 2.5 years), and are
less influenced by localised weather patterns and catchment runoff. Lake overturn in
most reservoirs occurs in June and July when surface water temperatures are at their
lowest (15–19°C).
Both reservoirs and weir pools throughout the Australian tropics and subtropics
regularly experience seasonal, cyanobacterial blooms (Fabbro & Duivenvoorden
1996; Harris & Baxter 1996; McGregor & Fabbro 2000). While both planktonic and
benthic cyanobacteria have been confirmed as toxigenic from Australian waters
(Table 1), the planktonic species remain the major concern to water managers (Fig 1).
4
Table 1. Toxigenic cyanobacteria known from Australian freshwaters
Species
Habitat*
Toxin
References
Anabaena circinalis Rabenhorst
F,P
saxitoxins
Humpage et al 1994,
Negri et al 1995, Negri
et al 2003
Aphanizomenon ovalisporum Forti
F,P
cylindrospermopsin,
deoxy-cylindrospermopsin
Shaw et al 1999
Cylindrospermopsis raciborskii
(Woloszynska) Seenaya & Subba
Raju
F,P
cylindrospermopsin,
deoxy-cylindrospermopsin
Hawkins et al 1985,
1997, Chiswell et al
1997, Norris et al 1999,
McGregor & Fabbro
2000, Saker & Neilan
2001
Lyngbya wollei (Farlow ex Gomont)
Speziale & Dyck
F,B
cylindrospermopsin,
deoxy-cylindrospermopsin
Seifert et al 2007
Limnothrix/Geitlerinema
F,P,B
unknown
Bernard et al 2010
Microcystis aeruginosa (Kützing)
Kützing
F,P
microcystins
Baker & Humpage
1994, Jones & Orr
1994, Jones et al 1995
Nodularia spumigena Mertens 1822
M,P,B
nodularin
Baker & Humpage
1994, Codd et al 1994,
Jones et al 1994,
Heresztyn & Nicholson
1997
Phormidium aff. amoenum Kützing
F,B
unknown
Baker et al 2001
Phormidium aff. formosum (Bory)
Anagnostidis & Komarek
F,B
unknown
Baker et al 2001
*F - Freshwater, M – Marine/Estuarine, B - Benthic, P – Planktonic
Fig 1. Toxigenic planktonic cyanobacteria known from Australian freshwaters, Anabaena circinalis (a),
Aphanizomenon ovalisporum (b - c), Cylindrospermopsis raciborskii (d), Microcystis aeruginosa.
In the sub-tropical/tropical regions of Australia, cylindrospermopsin-producing
cyanobacteria represent the predominant toxigenic taxa in the plankton.
Aphanizomenon ovalisporum was originally characterised as a producer of the
cyanotoxin cylindrospermopsin and its epimer deoxy-cylindrospermopsin in Australia
after a significant bloom was detected in newly constructed shallow lakes in subtropical Queensland (Shaw et al. 1999). This species isolated from Lake Kinneret,
Israel had previously been shown to produce cylindrospermopsin (Banker et al. 1997).
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A. ovalisporum has since been sporadically found in artificial lakes and reservoirs
throughout temperate and sub-tropical eastern Australia where it prefers warm,
stratified, high alkalinity/conductivity waters. Its close morphological affinity to
common planktonic species such as Anabaena bergii and
Anabaena aphanizomenoides, suggests a wider distribution in Australia than is
currently known. In northern Australian reservoirs maximum abundance generally
occurs between the months of October and May where it rarely occurs in
concentrations higher than ca. 20 000 cells mL-1. It has, however, been reported as
monoculture “blooms” forming brown surface scums from a number of eutrophic
artificial lakes adjoining housing estates. Little information is available on the global
distribution of A. ovalisporum, though it is known from northern and central Europe
(Quesada et al. 2006), the Middle East (Pollingher et al. 1998), and North America
(Yilmaz et al. 2009).
Cylindrospermopsis raciborskii is the most common and widespread toxigenic
cyanobacteria in northern Australia and has been recorded in approximately 86% of
all reservoirs sampled throughout this region. It shows a marked seasonal pattern of
abundance in all the reservoirs, however in general this is less pronounced in the weir
pools. The timing of peak seasonal abundance varies considerably between
reservoirs, and is largely related to latitude. Characteristically it is observed between
the months of December and February, corresponding to the period of peak summer
thermal maxima (McGregor & Fabbro 2000, Burford & O’Donohue 2006).
The genus Cylindrospermopsis Sennaya & Subba Raju contains eight species that
largely occupy a pantropical distribution. Generally they are characterised by solitary
trichomes often attenuated at one or either ends, with heterocysts developing in the
terminal position; akinetes are intercalary and develop para-heterocytically. Three
Cylindrospermopsis morphotypes are recognised from tropical and sub-tropical
Australian lakes and reservoirs, including the most common straight form, a coiled
form corresponding to C. philippinensis (Taylor) Komárek, and an irregular/sigmoidshaped form known from a number of shallow tropical reservoirs. This
morphological plasticity often leads to identification difficulties, particularly in
relation to morphologically allied species such as Raphidiopsis mediterranea.
Wallum habitats
The sandy lowlands of the Cooloola coast and sandmass islands of Fraser, Moreton,
Bribie and North Stradbroke support significant sub-tropical coastal wallum wetlands.
The region contains more than half the world’s perched dune lakes as well as
numerous window and barrage lakes. These herbaceous wetlands occur as complex
mosaics of lacustrine, riverine and palustrine systems comprising permanent and
ephemeral streams, lagoons and lakes and wet heath communities dominated by
sedgelands comprised of Lepironia articulata, Gahnia sieberiana, Eleocharis spp.,
and Baumea rubiginosa. Due to high levels of allochthonous humic deposition these
systems are typically acidic (pH <6), low salinity (50 – 100 μS cm-1), humic with low
levels of dissolved and suspended solids (TDS 75 – 120 mg L-1) and are generally
oligotrophic; their optical properties range from highly dystrophic to clear (LeeManwar et al. 1980, Bowling 1988).
These wallum areas support a diversity of acid adapted biota. Notably populations of
nationally and internationally threatened species such as the Oxleyan Pygmy Perch
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(Nannoperca oxleyana), Wallum rocket frog (Litoria freycineti), and the Wallum
sedge frog (Litoria olongburensis). Due to its proximity to the coast, wallum habitat
is under substantial threat from residential, industrial and agricultural development
consequently the resident biota are threatened by habitat loss and fragmentation.
Cyanobacteria are conspicuous constituents of the three dominant microphytic
assemblages of wallum habitats: phytoplankton, metaphyton (floating mats),
epiphyton (periphytic growths) and epipelon (benthic mats and films). Little is known
of the planktonic microalgae and cyanobacteria of these low pH systems, which are
typically dominated by chlorophytes, notably desmids and diatoms (Bayly et al. 1975,
Bowling 1988, Rott et al. 2006). The cyanobacterial microflora from these habitats
has been hitherto largely unknown. Eighteen south-east Queensland coastal wallum
wetland sites have been sampled as part of a larger project documenting north-eastern
Australia’s freshwater cyanobacterial flora (McGregor et al 2007, McGregor 2007).
Although lake productivity is typically low, colonial coccoid genera including
Aphanothece, Eucapsis, Rhabdoderma and Rhabdogloea dominate cyanobacterial
phytoplankton assemblages, particularly during the austral summer months of
December – February (Fig 2).
Fig 2. Blue Lake, North Stradbroke Island (a), Eucapsis sp. (b), Rhabdogloea ellipsoidea (c),
Rhabdoderma sp. (d), Chroococcus sp. (e).
Epipelon (benthic mats and biofilms) are often the most conspicuous microfloral
assemblages in palustrine systems and on stream and lake benthos. These
communities are taxonomically and structurally diverse and include the coccoid
genera Chroococcus, Gloeothece, Gloeocapsa, Cyanothece and Merismopedia,
filamentous non-heterocystous genera Geitlerinema, Leptolyngbya, Phormidium,
Komvophoron, Katagnymene and Scytonema, and filamentous heterocystous genera
Stigonema and Hapalosiphon. Emergent sedges in the littoral zone of streams, lakes
and swamps provide substantial vertical substrate for ephiphyton dominated by
Scytonema and Phormidium (Figs 3 – 5). However, members of the Nostocales
and Chroococcales are typically the predominant cyanobacteria in these habitats;
common genera include Scytonema, Hapalosiphon, Stigonema, Aphanothece,
Chroococcus, Merismopedia and Gloeothece.
Many of the cyanobacterial morphotypes from Australian wallum habitats identified
to date are either known from corresponding acidic “bog” wetland habitats from
7
central or northern Europe (e.g. Lederer & Soukupova 2002) or are likely to be unique
entities which require further investigations using combined molecular and
morphological criteria. The sensitivity of coastal wetland microflora including
cyanobacteria to changes in nutrient status and habitat fragmentation has been
demonstrated (Rejmánková et al. 2004). As such there is an urgent need to document
the endemic microflora to enhance our understanding of likely changes to increased
anthropogenic pressures.
Fig 3. Wallum habitat in Eighteen Mile Swamp, North Stradbroke Island (a), the emergent sedges
Lepironia articulata and Eleocharis spp. provides vertical habitat for epiphytic cyanobacterial
communities dominated by Scytonema and Phormidium (b), Scytonema spp. (c-d).
Fig 4. Lake Poona, South-east Queensland (a), epipelon communities dominated by filamentous green
algae, diatoms and desmids, and cyanobacteria including Katagnymene accurata (b 1-5) and
Merismopedia sphagnicola (c).
Fig 5. Wanggoolba Creek, Great Sandy National Park, Fraser Island (a), benthic cyanobacterial mat
community dominated by Komvophoron sp. (b 1-5), Cyanothece aeruginosa (c-d), and Phormidium
granulatum (e).
8
Thermal springs
Historically it was considered that thermally extreme environments (i.e. hot springs
and polar regions) harboured low microbial community diversity, and certainly early
studies based on morphological characters and enrichment studies yielded varying
estimates. Since the wider acceptance and application of molecular techniques we
have learned that the phylogenetic diversity contained in a single hot spring can span
the whole variety of microbial life (Hugenholtz et al. 1998), and that based on 16S
rRNA sequences the cyanoprokaryote component often spans a range comparable to
all known groups (i.e. Ferris et al. 1996).
Thermal springs characteristically have waters issuing at or above 36.7 oC (Pentecost
et al. 2003). Their dependent wetlands are distinctive ecosystems, particularly in arid
and semi-arid regions where they can represent one of the few permanent surface
water habitats in otherwise ephemeral settings (Fensham & Fairfax 2003). As well as
water permanence, these systems are typically characterized by high levels of
environmental constancy with respect to other physico-chemical conditions including
temperature, pH, and ionic composition. Thermal springs are therefore significant in
that they provide critical habitat for clusters of species, many of which are
ecologically restricted by narrow thermal tolerances.
In Australia, thermal springs provide habitat for a range of endemic biota including at
least 26 macroinvertebrate species (Ponder 1986, 1995; Ponder & Clarke 1990), four
fish species (Wager & Unmack 2000), and a number of aquatic macrophytes
(Fensham & Fairfax 2003). Although the microbial communities of these systems are
equally unique (Ling et al. 1989, Byers et al. 1998) there are few comprehensive
inventories or studies on their distribution and dynamics from Australian geothermal
systems. A study by McGregor & Rasmussen (2007) using a combination of
microscopic observation of morphological features, ultrastructural characterization,
and cultivation-independent molecular methods were conducted on an alkaline
thermal spring issuing at 43–71 oC in tropical North Queensland. The study revealed
unusual tentaculiform benthic mat communities dominated by fine filamentous
cyanobacteria, and associated with a variety of other cyanobacterial constituents
previously known as thermophilic from other continents (Fig 6).
Fig 6. Tentaculiform benthic cyanobacterial mats at Innot Hot Springs, Northern Australia (a),
Chroococcus thermalis (b), Mastigocladus laminosus (c), Leptolyngbya tentaculiformis (d),
Synechococcus lividus.
9
Eight genera and 10 species from three cyanobacterial orders were identified based on
morphological characters. The predominant order with respect to species richness and
relative biomass contribution was the Oscillatoriales with five of the 10 species. Fine
sections through the tentaculiform mats confirmed the dominance of the two
morphotypes corresponding to the genus Leptolyngbya, both of which had similar
ultrastructural features. DNA extracts made from sections of the tentaculiform towers
were analysed by 16S cyanobacteria-specific PCR and denaturing-gradient gel
electrophoresis yielded five significant bands which were identified and sequenced.
Generally the approaches yielded complementary information, however the results
suggest that species designation based on morphological and ultrastructural criteria
alone often fails to recognize their true phylogenetic position.
Based on morphological criteria the species richness at Innot Springs was far less than
reported from hot springs of other tropical areas. Sompong et al. (2005) recorded 19
genera and 36 species from nine thermal springs (30–80 oC) in northern Thailand;
Hindák (2001) 19 taxa of cyanobacteria from hot springs on the shore of Lake
Bogoria, Kenya. The location of the Innot Springs mats in Nettle Creek, which is
subject to seasonal spates of varying intensity associated with tropical monsoon
systems, rather than relative flow constancy, may account for this reduced richness.
Under these conditions it is likely that the annual hydrograph influences changes in
mat structure and composition by altering the contribution of the thermal water to the
total stream flow at the site over time and by exposing the mats to periodic high flow
spates with sufficient intensity to physically scour them from the stream bed.
Typically as disturbance frequency increases, both biomass and diversity of stream
periphyton is generally reduced (Biggs et al., 1998).
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