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17
Journal of the Royal Society of Western Australia, 101: 17–43, 2018
© Royal Society of Western Australia 2018
Microbiomes of Western Australian marine environments
CHARLIE M. PHELPS 1, RACHELE BERNASCONI 1, MELISSA DANKS 2, JOSEP M. GASOL 1,3,
ANNA J. M. HOPKINS 2, JACQUELYN JONES 4, CHRISTOPHER R. J. KAVAZOS 2,5, BELINDA
C. MARTIN 6, FLAVIA TARQUINIO 1, MEGAN J. HUGGETT 1,2,7 *
1 Centre for Marine Ecosystems Research, and 2 Centre for Ecosystem Management, School of Science, Edith Cowan University.
Perth, WA, Australia
3 Institut de Ciències del Mar, CSIC. Barcelona, Catalonia, Spain
4 Trace and Environmental Laboratory, Curtin University. Perth, WA, Australia
5 School of Biological, Earth and Environmental Sciences, The University of New South Wales. Sydney, NSW, Australia
6 School of Biological Sciences, The University of Western Australia. Perth, WA, Australia
7 School of Environmental and Life Sciences, The University of Newcastle. Ourimbah, NSW, Australia
*Corresponding author: megan.hugge@newcastle.edu.au
Abstract
Microbes are fundamentally important to the maintenance of all habitats, including those in the
ocean: they govern biogeochemical cycles, contribute to resistance from disease and nutritional
requirements of macroorganisms and provide enormous biological and genetic diversity. The
oceanic environment of the west coast of Australia is dominated by the Leeuwin Current, a
and stretches of the coastline host unique assortments of tropical and temperate species. Seawater
itself, as well as the benthic macroorganisms that inhabit ocean environments, form habitats such
including stromatolites, continental slopes and canyons and abyssal plain enviroments. These
environments, and the macroorganisms that inhabit them, are all intrinsically linked with highly
at understanding these critical organisms within Western Australia. Here we review the current
literature from the dominant coastal types (seagrass, coral, temperate macroalgae, vertebrates and
stromatolites) in Western Australia. The most well researched are pelagic habitats and those with
stromatolites, whereas data on all the other environments are slowly beginning to emerge. We urge
connectivity of coastal microorganisms in Western Australia.
KEYWORDS: Marine microbiome, Western Australia, coral, seagreass, bacterioplankton,
macroalgae
Manuscript received 24 July 2018; accepted 15 November 2018
INTRODUCTION
In terms of both abundance and diversity, all ecosystems
on Earth are dominated by microbes which, although
invisible to the naked eye, are essential for the
functioning of the biosphere. We collectively refer
to prokaryotes (bacteria and archaea), microscopic
eukaryotes (such as protists and fungi) and viruses as
“microbes”, all of which are abundant in every aquatic
environment. The global ocean prokaryotic biomass
alone is in the order of a petagram of carbon (1015 grams),
with ocean sediment harbouring up to ten times more
than this (Whitman et al., 1998). Microbes also colonise
biotic and abiotic surfaces in the marine environment
in the tissues of many marine organisms, performing
ecological functions essential to their hosts (see pull-out
microbiomes Egan et al., 2008).
The term ‘microbiome’ (from ‘microbe’ and ‘biome’)
refers to the microbes living on a specific habitat,
e.g., the ocean microbiome, which includes the water
microbiome, the sediment microbiome, the microbiome
of macroalgae, seagrasses, corals and sponges, as well
as the microbiomes of marine sh and marine mammals.
The microbiome also refers to the total genomic pool of the
microbiota. In host-associated microbiomes, this extends
the host’s functional genome well beyond its evolutionary
capabilities.
In addition to their enormous abundance, microbial
communities harbour a vast metabolic functional
chemical reactions including photosynthesis. As a
biogeochemical roles, and are likely to be responsible for
most, if not all, key transformations in global cycling of
carbon, nitrogen, phosphorus, sulphur and iron. About
half of the Earth’s primary production (i.e. the conversion
of atmospheric CO2 into organic substances within living
18
Journal of the Royal Society of Western Australia, 101, 2018
organisms) is in the ocean, with most of this (ca. 90%)
performed by microbes (Duarte & Cebrian, 1996; Field
et al., 1998). In addition, most of the global respiration
(i.e. the degradation of organic carbon into CO2) stems
from microbial processes (del Giorgio & Duarte, 2002).
This productivity sustains marine food webs and is
fundamental to many of the services of the world’s
oceans.
Understanding the diversity and ecology
of microbiomes has been facilitated by the recent
development of ‘omic’ approaches. These methodologies
are based on the cost-effective sequencing of either
the whole DNA of the community (metagenomics),
the whole mRNA (metatranscriptomics) or various
sequencing (typically the 16S rDNA for prokaryotes and
of sequence-based data and the dominance in both
abundance and diversity of microbes in oceans, we
with macro-organisms. There is mounting evidence
that the health of many marine organisms depends on
their associated microbiome (e.g., Zozaya-Valdés et al.,
2015 and Sweet & Bulling, 2017). In addition, the large
genomic diversity within oceanic microbes has a large
biotechnological potential (Arrieta et al., 2010; Arnaud-
Haond et al., 2011). Hence, there is a vital need to improve
our understanding of the diversity, function, resilience
and connectivity of microorganisms in the ocean.
MICROBIOMES OF WESTERN
AUSTRALIA
With more than 20 000 km of coastline (of which 12 000
correspond to the mainland and the rest to islands),
Western Australia has an estimated >300 000 km2 of
territorial waters, mostly over the continental shelf.
Under the Integrated Marine and Coastal Regionalisation
of Australia, this area can be divided either into several
large Provincial Bioregions, or into eighteen mesoscale
Bioregions (Fig. 1). Transitional zones, or biotones, are
represented by the bioregions located between provincial
at the limit of their distributions. Three provincial zones
and four associated biotones are represented along
the Western Australian Coast. There are 18 defined
bioregions located along the Western Australia coast,
Figure 1. Location of Integrated Marine and Coastal Regionalisation for Australia (IMCRA) Provincial and Meso-scale
Bioregions for the Western Australian Coast. Data Source: Commonwealth of Australia (2006). The warm southward
19
10 of which are located within the tropical waters of
the Northwest Province and Northwest Transition (Fig.
1). Across this large range of latitude (> 20° of latitude
from ca. 14°S to 36°S) average sea surface temperatures
(SST) vary from 28°C in the north to 17°C in the south.
In addition, the Western Australian coast ranges from
sandy microtidal sites in the southernmost parts, to
and island archipelagos that create structure and small-
scale variability.
Within Western Australian waters, a number of key
to affect the distribution and activity of microbes.
Both the pelagic and benthic environments of Western
Australia are conditioned by the water current that
transports warm tropical Indian Ocean waters along
to the coast from north to south and continues east
the Antarctic Circumpolar Current from the west and
is compressed towards the coast. In addition to these
parallel to the northern Western Australian coastline and
along the shelf, transporting warm, low salinity waters
from the Arafura Sea and Gulf of Carpentaria into the
parallel to the coast in the northern part of the coastline,
it in part pushes the Leeuwin Current towards the
coast. As a result, these warm waters found at southern
latitudes in Australia’s west coast set this coast apart from
the oceanographic dynamics of the west coasts of other
continents such as America or Africa. This creates unique
southern latitudes. Additionally, the Leeuwin Current
generates warm-core and cold-core eddies, the former
a mosaic of waters with differences in temperature,
phytoplankton and productivity (Waite et al., 2007;
Paterson et al., 2013).
In addition to the oceanographic dynamics the shelf is
water habitats (Jones et al., 2014). There are steep canyons
that connect the shelf with deep ocean. In particular the
Naturaliste Bioregion (Fig. 1), allows episodic upwelling
of nutrient-rich deep waters. Inshore lagoons are key
sites of high benthic productivity (including macroalgae
and seagrass). These lagoons support diverse and
endemic invertebrate and vertebrate species that include
Finally, in the coastal regions of Western Australia are
highly diverse, living stromatolites of various ages that
et
al., 2015).
We chose to focus this review on a variety of
Australian ecological features and the availability of
published literature (Fig. 2). These microbiomes include:
seagrass, coral, temperate macroalgal, vertebrate, benthic
mats and stromatolites and planktonic (free-living)
microbiomes (Fig. 3). In general, we have restricted
our review to shallow waters, given the comparatively
higher amount of research that has been focussed on
Figure 2. Number of journal articles published on marine microbes in Western Australia showing a) host/habitat they
Symbols from the Integration and Application Network (ian.umces.edu/symbols/).
C. M. Phelps et al.: Microbiomes of Western Australian marine environments
20
Journal of the Royal Society of Western Australia, 101, 2018
in Western Australia. There are also a variety of other
habitats and organisms (e.g., salt marshes, mangroves or
invertebrates such as sponges, molluscs and arthropods)
that are not included in our review due to scarcity
of data, even though we recognise that these are also
important components of the marine ecosystem. As it
will become clear, the microbial ecology of the oceans
surrounding Western Australia is poorly understood. We
postulate that a full understanding of life in the ocean
associations to themselves and larger eukaryotic hosts.
our understanding of the oceanic environments and
will facilitate development of techniques to be used as
health diagnosis tools for both ocean organisms and
environments.
Seagrass microbiomes
that are distributed along the coastlines of every
et al., 2007). Seagrasses
can be referred to as ‘ecosystem engineers’ (see pull-out
et al., 1994); they provide a multitude
of ecosystem services such as coastal protection
from erosion (Ackerman & Okubo, 1993), sediment
stabilisation (Gacia & Duarte, 2001) and represent a
habitat and source of food for a variety of organisms
(Staples et al., 1985; Heck et al., 2008; Bertelli & Unsworth,
2014). Seagrasses also sequester and store an estimated
19.9 Pg of organic carbon, (roughly 10–18% of the total
oceanic carbon sequestration; Fourqurean et al., 2012;
Lavery et al., 2013; Serrano et al., 2016).
Figure 3. Conceptual diagram of Western Australian microbiomes and the functional roles that microbial communities
play within each habitat. Symbols are from the Integration and Application Network (ian.umces.edu/symbols/).
21
The term ‘ecosystem engineer’ refers to an organism
that directly or indirectly modulates the availability of
resources (other than themselves) to other species,
by causing physical state changes in biotic or abiotic
materials, in so doing they modify, maintain and/or create an
ecosystem.
The seagrass meadows of Western Australia are
among the most diverse in the world, with 11 genera
and 26 species of seagrass that represent 36% of global
seagrass diversity (Short et al., 2007). Seagrasses in
Western Australia are distributed along a latitudinal
range, which stretches from 13°S to 35°S (Short et al.,
2007). These meadows cover an estimated 20 000 km2 (ca
43% of the total Australian seagrass area) and include
both temperate and tropical species (Kilminster et al.,
2015). Northern Western Australia is dominated by the
tropical species Thalassia hemprichii and Thalassodendron
ciliatum, which both have ranges that reach to 22°S, a
latitude that also corresponds to the northerly limit of
the temperate seagrass Amphibolis antarctica (Walker,
1989; Kirkman, 1997). Cymodocea angustata, Halodule
uninervis, Halophila spinulosa and Syringodium isoetifolium
reach south to Shark Bay at 26°S (Walker, 1991; Kirkman,
1997). Southern Western Australia is dominated by
Posidoniaceae with eight Posidonia species inhabiting
requirement of the species (Carruthers et al., 2007). Over
1000 research papers and books have been published
since the early 1980s on the ecology of Australian
seagrasses, with much of this research conducted along
Western Australia (York et al., 2017). Within Western
Australia, seagrasses play a central role in sustaining
the aquaculture industry (Hanson et al., 2005; Ince et
al
seagrass meadows provide foraging grounds for the
western rock lobster Panulirus cygnus
valued at an estimated AUD $200 million (De Lestang
et al., 2009). Seagrass wrack is also an important habitat
when it is deposited in surf zones where it sustains
various components of the coastal ecosystem by feeding
amphipods, copepods, birds, crabs and a variety of
1984; Hyndes & Lavery, 2005; Ince et al., 2007).
Despite the importance of seagrass meadows in
in their area across the State, largely as a result of coastal
development and climate change (Hyndes et al., 2016).
Bioregion, Fig. 1), 97% of the seagrass meadow (34 km2)
had been lost by 1978 due to development of heavy
and nutrients into the bay (Cambridge & McComb,
1984). Similarly, at Albany up to 66% of the seagrasses in
Princess Royal Harbour and up to 46% of the seagrasses
in Oyster Harbour (South Coast Bioregion; Fig. 1) have
and town sewage (Bastyan, 1986; Kirkman, 1987). In 2011,
a particularly strong marine heat wave event caused
damage to 36% of the seagrass meadow area in Shark Bay
(Arias-Ortiz et al., 2018). In most cases seagrasses have
failed to recover despite improvements in water quality
(Mohring & Rule, 2013; Fraser et al., 2016). This has led
for continued seagrass decline, as well as more focused
A central, but overlooked, component to
understanding drivers of seagrass decline is the role
of microbes living in association with their host as a
single biological unit also referred to as the ‘holobiont’
et al., 2017). Seagrass
tissues are colonised by a diverse microbiome that play
a critical role in their growth and health due to their
Bonet et al., 2016, Tarquinio et al., 2018), protection from
pathogens (Marhaeni et al., 2011, Supaphon et al., 2013),
Küsel et al., 2006) and production of phytohormones
that stimulate plant growth (Kurtz et al., 2003). For
and sulphate-reducing bacteria present in the roots may
supply up to a third of the nitrogen requirement by
of organic nitrogen (Welsh, 2000; Nielsen et al., 2001; Cole
& McGlathery, 2012). Seagrass epiphytic cyanobacteria
and fungi also represent a source of antimicrobial,
antifungal and antifouling molecules and can protect
seagrasses from pathogens and biofouling (Gleason &
Paulson, 1984; Supaphon et al., 2013; Mazard et al., 2016).
The term ‘holobiont’ refers to an assemblage of different
interacting organisms considered as a single unit. For
example, a host organism (such as seagrasses, sponge, sh
etc.) and the microbes that live in and on that host, and their
entire genetic repertoire.
Microbial populations respond rapidly to
environmental disturbance due to their fast generation
times (Allison & Martiny, 2008). Consequently,
monitoring their composition and activity can serve as
and ultimately declines in seagrass health. Despite
the globally recognised importance of microbiomes
to seagrass health, research on their microbiomes
is fundamentally lacking, particularly in regard to
seagrass microbiome research revealed that only three
of 58 studies worldwide were on Australian ecosystems
(Ugarelli et al., 2017). While this review was not
the many studies on Australian seagrass and the small
portion that focus on the microbiome.
Whereas few research articles have been published
on Western Australian seagrass microbiomes compared
to other host-associated microbiomes (Fig. 2), this
research has led to several important discoveries.
Research on temperate Posidonia sinuosa communities has
revealed the importance of leaf-associated microbiota in
translocating nitrogen into seagrass leaves (Tarquinio
et al., 2018).
than in the surrounding habitat, indicating that there is a
in a function traditionally considered to be dominated
by archaea (Tarquinio, 2017). This work suggests a
previously unrealised role of the leaf microbiome in
the abundance of seagrass habitats worldwide.
Other seagrass microbiome research in Western
Australia focusses on identifying links between above
ground disturbances to seagrasses and changes in the
C. M. Phelps et al.: Microbiomes of Western Australian marine environments
22
Journal of the Royal Society of Western Australia, 101, 2018
Western Australian tropical seagrass species (Martin
et al., 2018), and led to a reduction in the abundance of
et
al., 2017). Fraser et al
structure of the seagrass sediment microbiome. This
threshold coincided with a reduction in sediment pH,
possibly favouring microbes such as sulphate reducers
The spatial structure and colonisation pattern of
electron microscopy revealed that colonisation of
microbes on Posidonia australis 5
cells/cm2) than on Mediterranean Posidonia species (P.
sinuosa 5 cells/cm2 and P. oceanica 6 cells/
cm2), possibly due to the older age of the Mediterranean
species roots compared with their Western Australian
counterparts (García-Martínez et al., 2005). Scanning
electron microscopy also revealed that microbial root
colonisation of three tropical Shark Bay seagrasses was
highest in the root hair zone compared to other parts of
et
al., 2018). Transmission electron microscopy and light
microscopy also revealed fungal hyphae penetrating the
root cells of Western Australian Posidonia spp. (Kuo et
al., 1981) and the mesophyll shoot tissue of the seagrass
Zostera muelleri (Kuo et al
about fungi on seagrasses in the State.
associated with their own root tissues, but they may
immediate surrounding sediment (the rhizosphere),
which, like terrestrial plants, represents a hot spot of
microbial activity (Shieh & Yang, 1997). Rhizosphere
organic carbon by roots), but they may also profoundly
of coastal waters has been linked to major seagrass
phosphorus on decomposition and reduction processes
of sulphate reducing bacteria; leading to an increase
(Bagarinao, 1992; Borum et al., 2005; Holmer et al., 2006).
However, nutrient additions and elevated temperatures
decomposition of detritus from the seagrass Zostera
muelleri
et al., 2017). Further studies are needed to understand
the delicate equilibrium that regulates seagrass and
rhizosphere bacterial interactions.
Collectively, these studies represent the ‘tip of the
iceberg’ with regards to understanding the importance
of microbes in Western Australian seagrass ecosystems.
It is clear that there are large gaps in our knowledge
of the microbial ecology of seagrass ecosystems from
of seagrasses has been declining at an increasing rate
et al
based management, such as an improved understanding
of the role and diversity of eukaryotic microorganisms
associated with seagrasses, together with their resilience
to change, is essential (York et al., 2017). Priorities for
future research should include focusing on sediment
well as those involved in pathogen defence (York et al.,
2017). Given recent marine heat waves along the Western
Australian coast (Arias-Ortiz et al., 2018), understanding
associated microbiomes should also be a priority (Hyndes
et al., 2016) to improve our current knowledge of seagrass
die-off events and to help restorative efforts across
Western Australia.
Coral Microbiome
Globally, shallow-water coral reef systems represent one
ecosystems (Crossland et al., 1991; Moberg & Folke,
1999). Such reefs are mostly located in oligotrophic, intra-
tropical regions, where environmental characteristics (i.e.
salinity and temperature) lie within the range necessary
to support the growth of reef organisms (Kleypas et
al., 1999). However, Western Australian shallow coral
reefs also include fringing and atoll reefs found in the
transition zones between temperate and tropical waters
where mean water temperature ranges between 20 to
24°C, several degrees cooler than the optimal coral
reef temperatures of 23 to 29°C. These environmental
features have generated diverse habitats with unique
coral communities along the coast. The Ningaloo Reef,
reef fringing the west coast of the continent (Ningaloo
Bioregion, Fig. 1). Most other reefs in northern Western
Australia either suround offshore islands or are on
emergent points along the continental shelf where
waters are clearer than inshore regions (e.g., Rowley
Fig. 1). The most southerly reef-forming coral species
in Western Australia are found in the Abrolhos Islands
Bioregion (Fig. 1). Those reefs lie within a region of
convergence between temperate and tropical waters, and
macroalgae communities. Coral species are also present
as far south as the Leeuwin–Naturaliste Bioregion,
i.e., Rottnest Island, Geographe Bay and Recherche
Archipelago, but have a patchy distribution in these
& Marsh, 1988).
Shallow water corals are able to grow in otherwise
oligotrophic waters due to their ability to establish
mutualistic symbiotic relationships with unicellular
dinoflagellate algae of the Family Symbiodinaceae,
as well as with bacteria and archaea. Corals also host
fungi and viruses, whose functional roles are not well
understood (Rosenberg et al., 2007). Functionally,
coral-associated symbionts are involved in nutritional
phosphate production and solubilisation, degradation of
dimethylsulfoniopropionate (DMSP); bacterial cell–cell
chemical signalling (also known as quorum sensing);
Parker & Delia, 1997; Rosenberg et al., 2007; Siboni et
al., 2008; Sharp & Ritchie, 2012; Fournier, 2013). For
instance, through their ability to produce secondary
metabolites and nutrients (Lesser et al., 2007; Olson et
23
al., 2009; Howard et al., 2011; Raina et al., 2013), bacteria
Vibrio, Pseudomonas and
Cyanobacteria) are likely to contribute to the control of
Symbiodinaceae's growth, density and nutrition (Ritchie
& Smith, 1997; Lesser et al., 2007). Conversely, the ability
of the Symbiodinaceae to produce DMSP potentially
controls nutrient availability and consequently the
growth of bacterial populations, some of which may be
pathogenic (Curson et al., 2011; Raina et al., 2016; Raina et
al., 2017). Preliminary studies suggest a role for archaea
in the recycling of nitrogen within the coral host (Siboni
et al., 2008), whereas viruses may help in controlling
bacterial abundance in the coral mucus (Wood-Charlson
et al., 2015).
Most coral microbiome research across Australia
has been conducted on the iconic Great Barrier Reef, in
north eastern Australia, with far fewer investigations on
the west coast (Crabbe & Carlin, 2009; Ceh et al., 2011;
Ainsworth et al., 2015; Thompson et al., 2015a). However,
research from Western Australia. For instance, the
role of nitrogen transfer to coral larvae by two strains
of Gammaproteobacteria was investigated within the
cosmopolitan coral species Pocillopora damicornis via
nanoscale secondary ion mass spectrometry (Ceh et al.,
was increased nitrogen uptake, providing evidence
for the role of microbes in nutrient transfer during this
critical early life history phase (Ceh et al., 2013a). Two
Acropora tenuis, P. damicornis and Tubastrea faulkneri
and detected an increase in Alphaproteobacteria
after spawning, with the Roseobacter clade found to
be conspicuous in all three species after spawning,
suggesting they may play a role in coral reproduction
(Ceh et al., 2012). The second of these studies found
that A. tenuis (a broadcast spawning species), and P.
damicornis
microbial assemblages into the surrounding seawater
during spawning (Ceh et al., 2013b). In particular,
A. tenuis released, in decreasing order, Roseobacter,
Flavobacteriaceae, Alteromonas and Shewanella, again
implying a role for some Roseobacter in the reproductive
processes of corals. In contrast, P. damicornis released
Alteromonas, Vibrio, Shewanella and Marinomonas with only
minimal amounts of Roseobacter detected in the water
column post-spawning. These studies add to several
et al., 2009 and Sharp & Ritchie, 2012) and indicate the
presence of Alphaproteobacteria, and in particular
the Roseobacter clade, as key coral associates in either
spawning corals or early life-history stages.
distinct components of the coral holobiont in contrasting
coastline, Western Australia presents opportunities to
environmental conditions. Thomas et al
Symbiodinaceae community variation within Acropora
from the Kimberley region (mean SST from 26 to 31°C)
and the Abrolhos Islands (mean SST from 20 to 25°C),
whereas Ceh et al
bacteria in the coral species Pocillopora damicornis at
Island (mean SST from 19 to 23°C). Interestingly, both
studies found minimal variation in microbial community
structure despite the large distance between sampling
One possible mechanism for the similarity between
sampling regions may be the connectivity of Western
Australian reefs via oceanographic features (e.g., the
Leeuwin Current) that are likely to be the main pathways
connecting Symbiodinaceae and bacterial communities
of the tropical north with the temperate south regions
of Western Australia. With regards to Symbiodinaceae
communities in Western Australian Acropora corals,
Thomas et al. (2014) show that most colonies had a
association with clade G, in contrast to studies in other
regions where clade G has not been detected in Acropora.
A biogeographical study of bacteria and archaea
associated with the coral Stylophora pistillata from seven
major regions across the globe also showed unique
features of the holobiont in corals from Western Australia
(Neave et al., 2017): among these regions, only Western
Australian corals were found to host distinct lineages
of the coral-associated Gammaproteobacterial genus
Endozoicomonas. S. pistillata from Western Australia also
contained high numbers of Pseudomonas, not seen in other
regions. Although this comparison is based on just two
studies, taken together they suggest Western Australian
promoting the importance of Western Australian corals as
an endemic reservoir of microbial diversity.
Despite their isolation, Western Australian coral
reefs are not immune to climatic events and other
human related impacts. Large-scale disturbances (such
impact on Western Australian corals (Speed et al., 2013).
However, record temperatures of up to 5°C above long-
term averages during 2010/11 caused major bleaching
cover along parts of the Western Australian coast (Pearce
et al., 2011, Moore et al., 2012, Depczynski et al., 2013).
Local impacts of sedimentation due to dredging is also
an important environmental impact in Western Australia,
particularly in the Northwest Province Bioregion
(Jones et al., 2015). Increased sedimentation rates and
turbidity caused by dredging and deposition of dredge
spoil can reduce light available to Symbiodinaceae
for photosynthesis (Bessell-Browne et al., 2017), with
potential consequences for other components of the
coral microbiome, and as a result coral health. For
make corals more susceptible to disease and bleaching
events (Hughes et al., 2017), as well as reducing rates of
et al., 2012). However, the consequences of altered
environmental conditions on Western Australian coral
microbiomes are still poorly understood with regards to
diversity, abundance and functionality, including their
connection with coral health (Pollock et al., 2014).
Temperate macroalgal microbiomes
Temperate reefs, dominated by macroalgae, are
ecologically, culturally and economically important
(Harley et al., 2012). Macroalgae provide many essential
roles in marine ecosystems (Steneck et al., 2002), such as
C. M. Phelps et al.: Microbiomes of Western Australian marine environments
24
Journal of the Royal Society of Western Australia, 101, 2018
primary production, the provision of habitat (see pull-
ecosystem engineers, page 21), nutrient retention/
cycling, as well as CO2 storage (Egan et al., 2013; Koch
et al., 2013). Macroalgal growth, health, resilience and
with the associated microbiome (Case et al., 2011; Egan
et al., 2013). The relationship between microbes and
macroalgae can be mutually beneficial, parasitic, or
commensalistic (Armstrong et al., 2001; Case et al., 2011;
Abby et al
Kingdom using the green alga Ulva linza, found that
growth and morphology of seaweed, whereas algae
without these bacterial isolates displayed abnormal
growth and morphology (Marshall et al., 2006). Fungi
obligate symbioses, termed mycophycobioses, and have
been described in brown, red and green macroalgae
(Raghukumar, 2017). Overall, microbial communities
are an integral component of sustaining normal algal
function and are therefore important for the entire
macroalgal ecosystem (Burke et al., 2011).
Western Australian benthic reef ecosystems, from
the Northwest to the Southwest Province (Fig. 1), host
diverse assemblages of macroalgae (e.g., Huisman,
2018). An early study of macroalgal microbiomes
bacteriochlorophyll on various substrates, including
red and green species of macroalgae, and found high
abundances on Western Australian algae (Shiba et al.,
1991). More recently, the microbiome of the brown kelp,
Ecklonia radiata, was found to be stable in composition
among healthy individuals across the entire southern
coast of Australia (Marzinelli et al., 2015). The two
other studies of macroalgae microbiomes from Western
Australia indicate important ecological roles, including
being the main decomposers of beach wrack on Western
Australian sandy beaches (McLachlan, 1985) and cues for
et al., 2018).
There has been a substantial body of work on the
microbial ecology of several macroalgal species from
eastern Australian temperate waters, including several
species also present in Western Australia. These include
studies of the red alga, Delisea pulchra, and its role in
et al., 1998; Rasmussen et al
et al., 2002), as well as the ability of bacteria from the
green alga Ulva lactuca to prevent biofouling (Holmström
et al., 1996, Egan et al., 2000, Egan et al., 2001, Holmström
et al., 2002). Given the different oceanographic
of Australia’s east and west coasts and the high levels
macroalgal endemic species on the west coast, similar
studies on the western microbiomes are required.
In temperate Australian waters, including those in
the west, the brown kelp Ecklonia radiata is the dominant
habitat-forming alga (Kirkman, 1981). In recent years,
kelp distribution and biomass has declined on both
the east and west coastlines mainly due to rising water
temperature (Wernberg et al., 2011a) and associated
bleaching (loss of algal photosynthetic pigment) in this
species (Phelps et al., 2017). Some evidence suggests
that microbes could play a substantial role in the decline
of macroalgal biomass and habitat (Egan et al., 2014;
et al et al. (2015)
Ecklonia
radiata microbiomes along the temperate Australian
coastline (Marzinelli et al., 2015) and Ecklonia radiata
infected with a putatively pathogenic bacteria displayed
et al., 2017). These observations show
that the kelp microbiome is linked to both bleaching and
temperature and may play a direct role in decline of kelp
health.
The term ‘dysbiosis’ refers to a microbial community shift
that has a negative impact on the host.
Changes in environmental conditions such as sunlight,
chlorophyll-a, water temperature and salinity impact
the community structure of macroalgae microbiomes
(Gilbert et al., 2010). Future microbial studies should
environmental, biological and anthropological factors
on the Western Australian macroalgae holobiont. In
particular, rising seawater temperatures have been
cover and range contraction of many macroalga species
along this coastline (Wernberg et al., 2011b, 2016b)
of rising water temperatures on macroalgal microbiomes
is timely. Increasing urbanisation also has an impact
on macroalgal microbiomes, with the kelp growing
on harbours and other marine structures displaying
microbiomes similar to those found on diseased algae
(Marzinelli et al., 2018). Further research is needed to
reef health along the Western Australian coast.
Marine vertebrates
A number of endangered marine mammals live, or
migrate, along the west coast of Australia, including
blue and humpback whales, dugongs and sea lions. In
addition, Western Australian coastal waters support
microbiome research in the last decade. Mutualistic
relationships between microbes and vertebrate hosts
have evolved through co-evolutionary processes over
long periods (Bäckhed et al., 2005) and have been linked
to changes in host phylogeny (Colston & Jackson,
gastrointestinal tract and respiratory tract of vertebrates
are colonised by microbes (Montalban-Arques et al.,
2015). Within these microbial communities, selective
produce highly structured populations of microbiota
(Moeller & Ochman, 2014). Our understanding of the
metabolic capabilities of the microbiome and its role in
host health has been mostly advanced through molecular
studies involving humans and captive mammals (Colston
& Jackson, 2016). However, there are over 17 000 marine
vertebrate species (Appeltans et al., 2012) and most of
microbiome research.
25
(Larsen et al., 2013, Lowrey et al., 2015), whales (Apprill
et al., 2014, 2017), dolphins and sea lions (Bik et al., 2016).
Microbial communities are further structured according
vertebrate hosts, with the gastrointestinal (GI) tract the
the most studied, especially for commercially important
overall composition of the GI microbiome (Ingerslev et
al., 2014), but the homeostatic composition is continually
modified by interconnecting factors including host
pH, temperature), and microbial inhabitants (competitive
inhibition, metabolic activity). If the community
composition is altered, and key microbial members are
dysbiosis
such as metabolic functioning (Ríos-Covián et al., 2016),
et al
may progress (Montalban-Arques et al., 2015). Infections
are common among marine mammals (Nelson et al.,
2015), and the role of the resident microbiota in the
etiology of these conditions is poorly understood.
Dysbiosis is a relatively new way of considering disease
progression, and, as disease is one of the main causes of
death in marine mammals (Waltzek et al., 2012), it may
be an important focus for marine vertebrate microbiome
research.
associated with marine mammals has not been studied
within Western Australian populations. Healthy
humpback whales from the North Atlantic, North
dominated by specific bacteria (Tenacibaculum and
Psychrobacter) that is greatly reduced on entangled or
deceased whales (Apprill et al., 2014). On the east coast of
Australia, faecal microbiomes from captive dugongs are
less diverse than those of wild dugongs and are missing
many bacterial members that dominate the wild dugong
microbiome (Eigeland et al., 2012). Delport et al., (2016)
found a similar result in wild and captive Australian
sea lions and presumed for both cases that contrasting
diets between wild and captive animals played a key
Furthermore, the captive dugongs were orphaned at
one and three weeks, so it is possible they may not have
microbiome (Eigeland et al., 2012). It would be valuable
west coast wild and captive vertebrates as well as
their east coast counterparts to further understand the
structure of Western Australian vertebrate microbiomess.
In particular, respiratory microbiomes are likely to be a
useful target as the respiratory tract is one of the most
et al., 2017),
(Thomas et al., 2016). Conducting similar research on
be of particular importance.
Despite the requirement for long-term protection
of sea turtles, the microbiome of Western Australian
the Indian Oceans largest population of hawksbill turtle,
have not been described (Pendoley et al., 2016). Sea turtles
from an early age and rely heavily on the hindgut
microbial fermentation for digestion. The gut microbiota
dietary factors which change as the turtles mature from
juvenile to adult (Price et al., 2017). Building on this work,
of marine hindgut fermenters, particularly in terms of
dietary requirements, would be relevant for rehabilitation
and protection programs in Western Australia.
Finally, aquaculture is an important economic
development in Western Australia, with production
Midwest Aquaculture development zone, declared in
Coast Bioregion (Fig. 1). A number of tropical native
species are raised in aquaculture, and one of the greatest
challenges they face is bacterial disease, with most
bacterial species isolated from Australian aquaculture
environments (including those from Western Australia)
presenting antibiotic resistance (Akinbowale et al.,
2006). Due to the broad target range of antibiotics, both
lead to dysbiosis, immune suppression and possibly an
et al., 2016).
As an alternative, probiotics and prebiotics are being
in aquatic animals (Banerjee & Ray, 2017). Probiotics have
host as a healthy microbiome (immune system, nutrition,
reports that probiotics are not fully retained (Akhter et
al., 2015). The increasing demand for sustainable seafood
and the growing Australian population means the health
management within aquaculture must be a top priority if
The high biodiversity and endemism of Western
place to study marine vertebrate microbiomes and with
the past warming anomalies in sea surface temperature,
of the microbiome can be studied within a single species
in the wild. Both captive animals, and model systems
functional role of the microbiome, improving our
understanding of co-evolutionary mechanisms that
in the natural environment, the resilience and metabolic
a single host species, eliminating variation caused by
into a new environment, key questions arise such as: will
the microbiome be restructured by the new metabolites
and populated by new seeding bacteria, or can the same
species persist by changing their metabolic output? Such
species along the Western Australian coast such as
Choerodon rubescens (Cure, 2018), and Chaetodon assarius
C. M. Phelps et al.: Microbiomes of Western Australian marine environments
26
Journal of the Royal Society of Western Australia, 101, 2018
(Wernberg, 2012), and comparing the microbiome from
distinct populations over large distances. Furthermore,
researchers could track the movement of potential
pathogens from historic to new populations, which could
understanding of the relationship between dysbiosis and
disease in marine vertebrates.
Plankton microbiome
Seawater is amongst the most abundant compounds
on the Earth’s surface, covering more than 70% of the
viruses, 1 million prokaryotic cells and 1000 unicellular
eukaryotes (e.g., Kirchman, 2008). In addition to their
enormous biomass, planktonic microorganisms also
biogeochemical transformations including the nitrogen
and carbon cycles (Falkowski et al., 1998). While recent
‘omics technologies and global ocean surveys (e.g.,
Sunagawa et al., 2015 and Yooseph et al., 2007) have
greatly facilitated our knowledge of global oceanographic
oceanic microbial community diversity and function
remain a global challenge. In spite of that, we know very
marine waters, in what abundances, what are the drivers
of planktonic microorganism abundance, activity or
Within Western Australian waters, phytoplankton,
be investigated among the planktonic marine microbes,
possibly because measures of chlorophyll-a concentration,
an indicator of phytoplankton biomass, were an easy way
of characterising the trophic conditions of an aquatic
environment. Conspicuous eukaryotic phytoplankton
as well as the phytoplankton of Western Australian
estuaries (John, 1983). Recent syntheses of phytoplankton
abundance and biomass (Davies et al., 2016) and
chlorophyll-a measurements (Davies et al., 2018) around
Australia have been published, and the data made
public through the Australian Ocean Data Network
system (http://portal.aodn.org.au/). Comparison of
chlorophyll (0.14 to 0.25 µg Chl a l–1 in the west, about
half the annually integrated value in the east (Thompson
et al., 2011). The Southwest coast has also been shown to
have relatively few smaller eukaryotes (pelagophytes,
prasinophytes, cryptophytes, chlorophytes) and fewer
larger eukaryotes (bacillariophytes and dinophytes)
boundary currents, the vertical stability of the water
column, and the average availability of nutrients in the
euphotic zone (Blondeau-Patissier et al., 2011).
In particular, there are few records of
picophytoplankton (cyanobacteria of the genera
Prochlorococcus and Synechococcus, as well as small
eukaryotes) in Western Australia. Thompson & Bonham
cyanobacteria in the Kimberly region and a recent study
similar amounts of the two cyanobacterial groups, and
about one order of magnitude fewer picoeukaryotes
(Thomson & Pattiaratchi, 2018). The study reports
little seasonality in picophytoplankton abundance,
and suggests that their abundance increases following
marine heat waves. These microbes are good markers
of long-term tropicalization as Prochlorococcus prefers
warmer temperatures and less nutrients (Li, 2009).
They also indicate oceanographic features, such as the
warm-core eddy linking Leeuwin Current, shelf and
Paterson et al. (2013). A study of their relative abundances
between El Niño and La Niña periods (July 2009 – June
2010 vs La Niña of July 2010 – June 2011) showed
increased abundances of cyanobacteria, and particularly
of Prochlorococcus
regions, indicating a general tropicalization of the waters
(Thompson et al., 2015b).
Despite the abundance, activity, diversity and trophic
role of the heterotrophic prokaryotes as essential
carbon cycle (Whitman et al
et
al. (2011) enumerated bacterioplankton, virioplankton
and picoautotrophs across the Ningaloo Reef and into the
sandy lagoon and also measured active depletion through
the coral reef of all groups. They found that Synechococcus
removal was biogeochemically more relevant, in terms
coral than the other microbial groups. Jones et al. (2014)
compared the abundances of bacteria, picophytoplankton
Collier Bay, north of Broome. They observed a mosaic
of concentrations with abundances typical of a tropical
4 Synechococcus 5 6
viruses, with a larger variability in viruses), with lower
abundances near the coast where waters were more
turbid.
In terms of diversity, Raes et al. (2014) used a
fingerprinting approach to study bacterioplankton
community composition across a large latitude gradient
(10°S to 32°S) following the continental shelf break from
The authors found that bacterial communities were
study Raes et al. (2018), used tag sequencing to show a
powerful diversity gradient between the northernmost
area, characterised by high temperatures and low
diversity, and the lowermost area, characterised by
lower temperatures and higher diversity. Bacterial
richness almost doubled between the two areas, and was
positively correlated to total dissolved inorganic nitrogen,
chlorophyll-a, phytoplankton community structure,
and primary productivity. Further analysis of these data
(Raes et al
dominated by the same groups (SAR11, Synechococcus,
Flavobacteriaceae, Rhodobacteraceae, etc.) in similar
into three groups, according to whether they originated
in the Timor Sea, the subtropical waters, or the Leeuwin
27
Figure 4. Overview of the microbiome community composition of water samples collected in Western Australia and
the IMOS National Reference site. Wreck Rock is a shallow (~5 m deep) rocky coastal site and Centaur Reef (~10 m deep)
for deep (46 m) samples or split into summer (January–April) and winter (July–September) months (surface data only).
Sequences of metazoa and macroalgae were removed from panel A.
C. M. Phelps et al.: Microbiomes of Western Australian marine environments
28
Journal of the Royal Society of Western Australia, 101, 2018
cold-core eddies and shelf waters. In their studies of the
oceanic nitrogen cycle, these authors also measured the
diversity of the nifH et al.,
2018), and the nosZ gene (N2
et al., 2016) in the same transect cited
above. Most nifH genes were from Gammaproteobacteria
and not correlated to the latitude and temperature
gradient, while most of the nosZ genes belonged to the
Roseobacteraceae and were more abundant in the warm
areas. Total bacterial abundance was also positively
related to temperature.
More recently, the BioPlatforms Australia initiative on
Marine Microbes (BPA-MM) sequenced 138 samples from
134 at two more coastal sites (Wreck Rock and Centaur
Reef) each month for one year. (Brown et al., 2018). About
7 sequences. On average, these communities
were dominated by the SAR11 Alphaproteobacteria
and Bacteroidetes with relatively low numbers of
Gammaproteobacteria. Bacteroidetes and Roseobacterales
were more relevant at the coastal stations while more
“oceanic” bacteria, such as Prochlorococcus, SAR234
structure. These data from represent critical baselines
that can be utilised to measure and predict changes in
microbial community structure under future local and
global environmental change (Brown et al., 2018).
Despite our limited knowledge of prokaryotes
in Western Australian waters, even less is known of
microzooplankton biomass and grazing activity (e.g.,
Paterson et al., 2007), but there are no reports we are
aware of about small protist diversity or even abundances
in Western Australia. The BPA-MM project used 18S
rDNA sequencing of eukaryotes collected on 0.2 µm
et al., 2018).
and at the two coastal sites of Centaur Reef and Wreck
metaphyta. Chlorophyta (in particular Mamiellophyceae),
species) and Stramenopiles (in particular Diatoms)
dominate the communities, with, again, differences
diversity data or any mycoplankton data for Western
Australian waters.
In estuaries and coastal lagoons, bacterioplankton
and their connectivity to terrestrial inputs (e.g., Yeo et
al.,
ocean, but many coastal lagoons are also connected
either by storm-related seawater inputs, or by seawater
2005; Kavazos et al
bacteria, protists, fungi and viruses in Western Australian
estuaries, although the (large and conspicuous)
bacterial diversity in water bodies of the Lake MacLeod
basin indicated a large degree of between-lake microbial
community variability with each pond despite similarities
in size, environment and position in the landscape
et al
sediment bacterial and ciliate communities (Kavazos et
al., 2018). A variety of previously unknown microbial
et al., 2017) consistent with
the seawater nurturing these environments (Kavazos
et al., 2017). These data add to ideas that identify
microorganisms as important players in coastal (carbon,
but also species) connectivity and spatial subsidies.
habitats and probably also influence coastal water
bodies (e.g., Säwström et al., 2016) and thus support the
incorporation of microbial oceanography into future
studies of the Western Australian oceanic environment.
Benthic microbial mats
Sedimentary biofilms, or microbial mats, have been
present throughout most of the geological history
of Earth (Edgcomb et al., 2014; Ruvindy et al., 2016).
Microbial mats have had important impacts on past
biogeochemical cycles and continue to persist particularly
in hypersaline regions around the world. Microbial mats
are composed of layers, where each layer is dominated
by different microbial metabolic processes that are
et al.,
(Kunin et al., 2008; Baumgartner et al., 2009; Dupraz et al.,
2009; Schneider et al., 2013; Pages et al., 2014). Western
Australian coastal environment supports a diverse range
of microbial mats, both lithifying and non-lithifying, and
represents one of the most well-studied microbiomes in
the State (Fig. 2).
Stromatolites, a form of microbial mat, are often
referred to as living rocks as they form conspicuous
The greatest diversity of stromatolites on the planet
is found along the Western Australian coast, which
makes it an important region for modern stromatolite
research. Stromatolites represent modern analogues
of the ancient microbial communities, which formed
the earliest known biosphere during the Archean,
some 3.5 billion years ago (Grotzinger & Knoll, 1999).
Stromatolites are typically domal organo-sedimentary
deposits with planar to sub-planar laminae formed by a
1987). Thrombolitic stromatolites, on the other hand, are
of similar benthic bacterial origin but lack the internal
laminae (Aitken, 1967). Stromatolites are mostly found in
Western Australian coastal lake systems and embayments
aragonite precipitation. It has also been hypothesised
29
(Playford & Cockbain, 1976, Macintyre et al., 1996,
Steneck et al., 1998), although predation by protozoan
Qassab et al., 2002).
The intertidal and subtidal areas of the Shark
Bay Bioregion (Fig. 1) provide suitable habitats for
stromatolites, which occupy over 600 km2 (Jahnert
& Collins, 2012; Collins & Jahnert, 2014). Because of
most well studied in Western Australia. Early work
concentrated on the intertidal stromatolites (Logan &
Cebulski, 1970; Logan et al., 1974; Playford & Cockbain,
1976), but recent work has also documented the
distribution and morphology of subtidal structures (Reid
et al., 2003; Jahnert & Collins, 2011, 2012, 2013; Collins
& Jahnert, 2014). Within Shark Bay, and particularly
Hamelin Pool, there are a diverse range of morphological
forms which have largely been described by Jahnert &
mats in the supra- and inter-tidal regions and smooth,
colloform and pavement structures in the subtidal region.
The different structures consist of several microbial
communities in which filamentous cyanobacteria
dominate blister, tufted and smooth structures, and
coccoid cyanobacteria bacteria dominate pustular,
colloform and pavement structures (Jahnert & Collins,
2013).
Broadly, stromatolite development consists of three
phases in which different filamentous and coccoid
cyanobacterial communities alternate as a consequence
et al., 2000).
These three phases have distinct microbial communities
that have been referred to as pioneer communities,
(Reid et al., 2000), where changes in sedimentation cause
Pioneer communities are distinguished by a population
carbonate sediment grains, embedding the grains to
the surface of the stromatolite. Pioneer communities
probably account for 70% of the growth stage cycle
and persist during sediment accretion. The bacterial
community, establishes when sedimentation ceases and
and cementation of silty carbonate material that have
community represents a mature bacterial biofilm
community consisting mainly of coccoid cyanobacteria.
the embedded carbonate sand grains and fuse adjacent
grains. This phase represents a period of high metabolic
activity which enhances aragonite precipitation and
formation of the distinctive stromatolite structures.
The fusing of sediment grains and aragonite formation
further develops the carbonate crust which persists into
the subsurface and facilitates further development of
the stromatolite. This process, however, is unlikely to
and intertidal stromatolites have slightly different
morphogenesis characteristics (Reid et al., 2003).
Nonetheless, the process of sediment entrapment by
biofilm lithification appears common to stromatolite
development (Grey et al., 1990; Moore & Burne, 1994;
Jahnert & Collins, 2012).
Many coastal lakes in Western Australia provide other
habitats for stromatolites, although they have received
northernmost of these habitats are the Northern Ponds of
Lake MacLeod (Shark Bay Bioregion; Fig. 1) where some
of the ponds contain colloform stromatolites (Logan,
1987; Shepherd, 1990). The MacLeod basin also contains
found in the supratidal and intertidal regions of Shark
Bay (Logan, 1987; Shepherd, 1990; Kavazos & Horwitz,
2016). Lake Thetis, near Cervantes (Central West Coast
Bioregion; Fig. 1), contains stromatolites that closely
resemble the dome structures found in the Precambrian
fossil record (Grey et al., 1990; Grey & Planavsky, 2009). In
Bioregion; Fig. 1), large thrombolitic stromatolites inhabit
the shallow waters (Moore, 1993; Moore & Burne, 1994).
Similar to stromatolites, the thrombolites are composed
et al
(John et al., 2009) by facilitating development of calcium
carbonate minerals; aragonite and stevensite (Burne et
al
microbial–metazoan relationship, which includes
amphipods and isopods grazing on the microbialite
structure (Konishi et al., 2001).
Stromatolites are found in other lakes along the
Western Australian coast, including Government
et
al., 2009), Pink Lake near Esperance (Burne & Moore
1987), and near Rockingham in Lake Richmond
(Kenneally et al., 1987, Chilton et al., 2012) and Lake
Walyungup (Coshell et al., 1998). These lakes are
susceptible to anthropogenic impacts largely because
of the degradation within their catchment regions from
urban development and agricultural use. Salinity and
et al
cyanobacteria essential to the growth of the thrombolite
structure (Smith et al., 2010).
Recent phylogenetic analyses of Shark Bay
stromatolites have identified a diverse community
of cyanobacteria, archaea and sulphate-reducing
bacteria (Goh et al., 2009). Specifically, Alpha- and
Gammaproteobacteria are highly abundant in Shark Bay
stromatolites and cyanobacterial communities where
they are represented by species of Euhalotheca, Gloeocapsa,
Gloeotheca, Chroococcidiopsis, Dermacarpella, Acaryochloris,
Geitlerinema and Schizothrix (Goh et al., 2009). Typically,
the surface mats are dominated by cyanobacteria (Garby
et al., 2013), although members of Alphaproteobacteria
and Bacteroidetes have also been detected on the
surface of smooth and pustular mats (Wong et al.,
2015). Recently, a new photosynthetic pigment,
chlorophyll-f, was discovered in the cyanobacteria
Halomicronema hongdechloris (Li et al., 2014). Archaea,
C. M. Phelps et al.: Microbiomes of Western Australian marine environments
30
Journal of the Royal Society of Western Australia, 101, 2018
represented by members of Methanomicrobiales,
Methanosarcinales, Methanococcales, Methanobacteriales,
Methanomassiliicoccaceae, Halobacteria (Goh et al.,
2006; Allen et al., 2008) and Parvarchaeota (Wong et al.,
2017), are abundant in Shark Bay stromatolites (Burns et
al., 2004) and likely have critical roles in the metabolic
pathways within the microbialite communities (Ruvindy
et al., 2016). Despite the importance of microbial
environments along Western Australia’s coastline, their
ecologies are poorly researched. This is a serious omission
considering the important roles these communities play
in the biogeochemical cycling of many essential elements.
There is a critical need to understand the functioning and
within microbial communities as such studies will
continue to reveal novel ecological processes, metabolic
pathways and biologically important molecules.
MICROBIOMES AND ENVIRONMENTAL
CHANGE
Oceans are critical for many ecological and economic
activites: they are valuable in climate regulation,
gases, recreation and culture, aquaculture, biodiversity,
conservation, biogeochemical cycling and provision
of pharmaceuticals. In Australia, the combined value
of the benefits that oceans will provide by 2025 is
(Ocean Policy Science Advisory Group, 2013). Despite
their tremendous importance, marine ecosystems are
currently facing unprecedented environmental change
and increasing frequency and intensity of cyclones,
storm events and heat waves. The critical nature of these
issues has led many marine scientists to focus research
on understanding, predicting, modelling and mitigating
the outcomes of global and local stressors to oceans.
Studies from Western Australia have led the world in
some of these areas with seminal work on oceanographic
modelling (Feng et al., 2003, 2013; Lowe & Falter, 2015),
et al., 2017),
tropicalization of temperate systems (Wernberg et al.,
2011a, 2016a) and thermal tolerance and recovery of coral
reefs (Gilmour et al., 2013; Schoepf et al., 2015).
On a regional scale, Western Australian coastal zones
are subject to many of the concerns that face the global
ocean, with notable environmental changes in the State
such as increasingly frequent heat waves (Feng et al.,
resuspension from dredge activities (Jones et al., 2015). In
situ temperature measurements at a coastal monitoring
station on the State’s continental shelf have shown a
mean temperature rise of 0.013°C year since 1951,
corresponding to ~0.6°C over the past five decades.
Measurements from three other shallow stations between
1985 and 2004 indicated even higher warming trends of
0.026 – 0.034°C year (Pearce & Feng, 2007). Recorded
impacts of environmental changes to coastal services
in Western Australia include widespread mortality of
et al., 2011) resulting in
et al., 2014), range
macroalgae (Wernberg et al., 2011b, 2013), tropicalization
of temperate regions (Vergés et al., 2014) and substantial
loss of seagrass and coral habitat (Fraser et al., 2014; Fig.
suggests that tropicalization of the ocean reduces
bacterial diversity (Raes et al., 2018) and many of the key
functional roles of microbial communities are altered
(Webster et alet al., 2018, Westwood et al.,
2018).
An important component for understanding the
response of marine systems to environmental change are
to observe likely impacts of environmental change
responses by marine communities where variation
in multiple factors (warming, heat waves, trophic
of temperature on marine ecosystems, due to the steady
temperature gradients and the lack of other stressors such
upwelling (Smale et al
in the Kimberley region may also provide an important
natural system in which to study genetic adaptation to
heat stress (Camp et al
studies (Wernberg et al., 2012; Cornwall & Hurd, 2015) as
discrete changes under controlled conditions can provide
essential data on the impacts of environmental change.
Given that microbes have rapid generation times they are
and are thus critical for incorporation into management,
early warning and modelling of the response of marine
ecosystems to environmental change.
Whereas microbiomes have mostly been overlooked,
field and aquaria-based studies of marine microbial
responses to environmental change in Western Australia
are beginning to emerge. For instance, Luter et al., (2015)
sponge Carteriospongia foliascens and concluded that light
Siganus fuscescens has been
is now common on southern reefs in both the east and
west of the continent. A biogeographic analysis of the gut
microbiome of wild populations of S. fuscescens across
over 2000 km of Western Australia’s coastline indicates
between populations, there is a persistent and abundant
microbial community in all populations. In addition,
short chain fatty acid production by their microbial
community is comparable in some tropical and temperate
populations, suggesting that this fish is well suited
to its new environment (Jones et al., 2018). Aquaria-
based studies testing the direct response of microbial
communities are also emerging; some of these are based
directly on key Western Australian benthic microbiomes
et al., 2018) whereas others are focused on
responses by populations from the east coast (Pineda
31
Figure 5. Summary of predicted environmental changes to key habitats from Western Australia. a) illustrates the state
edu/symbols/)
C. M. Phelps et al.: Microbiomes of Western Australian marine environments
32
Journal of the Royal Society of Western Australia, 101, 2018
et al., 2017). These studies indicate that temperature,
substantial impacts to microbiomes in the State’s benthic
marine ecosystems and enable us to understand the
processes that underpin the persistence of some species
and the decline of others under environmental change.
Encouragingly, the largest marine science research
organisation in the State, the Western Australian Marine
enhanced
understanding of the marine microbial systems that underpin
all marine biological activity in the Western Australian marine
environments” as a high priority for future research to be
addressed by year 2020. In addition, the BPA-MM project
microbes) is the focus of a long-term monitoring program
and pelagic sites across Australia, (Fig. 4). The BPA-MM
program is of a world-class standard and will provide
critical data facilitating our ability to predict potential
climate impacts (Webster & Bourne, 2012). Microbes
respond quickly to alterations of the environment
and we can now determine the structure of microbial
communities relatively simply and easily. Therefore,
the development of microbial indicator species and
of environmental stress and ecosystem health, both in
water (Ferrera et al., 2016) and microbiomes of other
organisms (Glasl et al., 2017), is a viable and achievable
goal. Incorporation of microbial ecology within marine
research and management is now urgent for the State.
CONCLUSIONS
We anticipate that the coming years will uncover
additional fundamental knowledge of microbes from the
west coast of Australia. This review highlights that this
coastline is vast, encompassing a wide range of marine
habitats, with unique features due to the attendant
currents in the region. There are many reasons why
marine microbial studies are lacking: the isolation of
the coastline, the large distances that it encompasses,
the difficulties in reaching remote coastal areas, the
the southern region and the substantial tides in the
north. Whereas there remain challenges to studying
these coastal environments, we conclude by highlighting
that the region has been home to some influential
et al.
symbionts of sponges could be passed directly from
parent to offspring via vertical transmission. These
cyanobacterial symbionts from mesophotic temperate
sponges (Keesing et al., 2012) and have provided one
of the few reports of the microbial assemblages of any
calcarean sponge (Fromont et al., 2016). Furthermore,
a recent environmental DNA (eDNA) study in Coral
Bay, intended to identify all organisms across the
Tree of Life, including bacteria and eukaryotes, uses
metagenomics and metabarcoding (Stat et al., 2017). The
metagenomics approach recovered mostly bacteria, while
the metabarcoding approach uncovered 2000 sequences
metabarcoding approach was much more informative,
revealing comparatively more biodiversity than
the promise of these techniques and their usefulness as
growth in the understanding of the abundance, diversity
and importance of microbes via the new generations of
‘omics technologies. Now we are poised on the edge of
new era that moves from the discovery of organisms
and their genes to the incorporation of ‘omics’ within
bench work. This era will forge new, multidisciplinary
datasets that will undoubtedly uncover even more of the
remarkable capabilities of the microbes of our planet.
Western Australia is one of the most isolated and pristine
coastlines on the earth, provides a steady gradient of
temperature and, uniquely, co-hosts both tropical and
temperate organisms for much of the coastline. Whereas
much of the basic work remains to be done, we argue that
this region also presents an unparalleled opportunity for
ACKNOWLEDGEMENTS
We thank J. Raes for access to his unpublished
of data for Figure 4. These data were accessed from
https://data.bioplatforms.com/organization/pages/
australian-microbiome/tools, which is a contribution of
the Marine Microbes (MM) and Biomes of Australian Soil
Environments (BASE) projects, through the Australian
Microbiome Initiative. The Australian Microbiome
Initiative is supported by funding from Bioplatforms
Australia through the Australian Government National
Collaborative Research Infrastructure Strategy (NCRIS).
We thank L. Bodrossy, T. Thomas, A. Fitzgerald and
David Haig is thanked for the supporting F. Evans to
“Landscapes, Seascapes and Biota: Unique Western
Australia – Past, Present and Future” associated with this
publication.
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APPENDIX 1
Meta-analysis references for Figure 2.
Articles were searched using the University of Western Australia’s OneSearch (accessed January 2018), which searches
across multiple databases including ISI Web of Science, Scopus, ScienceDirect, and PubMed. Articles were searched using
the terms: microbiome/microorganisms/microbes + (“host”) + Western Australia and manually checked for relevance.
Additional articles were also added when uncovered during the preparation of this review.
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