Factors Affecting Algae Biofilm Growth and Lipid Production - A Review

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Factors affecting algae biofilm growth and lipid

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ARTICLE in RENEWABLE AND SUSTAINABLE ENERGY REVIEWS DECEMBER 2015
Impact Factor: 5.9 DOI: 10.1016/j.rser.2015.07.090
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Renewable and Sustainable Energy Reviews 52 (2015) 418429
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Factors affecting algae biolm growth and lipid production: A review

Peter J. Schnurr, D. Grant Allen n
Department of Chemical Engineering & Applied Chemistry, University of Toronto, 200 College Street, Toronto, Ontario, Canada M5S 3E5
art ic l e i nf o
a b s t r a c t
Article history:
Received 21 May 2015
Received in revised form
7 July 2015
Accepted 17 July 2015
Algae is recognized as a potentially valuable source of biofuels and biochemicals; however, a major
limitation to commercialization is in the high cost of harvesting, de-watering, and downstream
processing of dilute algae biomass when it is grown planktonically. Growing algae as a biolm offers
potential advantages for biomass processing because biolms are immobilized and orders of magnitude
more concentrated. For these reasons there has been an emerging interest in algae biolm biofuel
research over the past several years. Additionally, there has been a considerable amount of work on
understanding algae biolms in nature, and on using algae biolms for tertiary wastewater treatment.
This review paper draws from all of this literature to describe algae biolm composition, and their
growth responses to the key environmental factors affecting growth and internal lipid concentrations;
the emphasis being on optimizing biomass and lipid productivity. Additionally, the paper summarizes
key things known about planktonic algae growth and bacterial biolm growth in order to make
inferences about the potential growth of algae biolms. The paper identies many key knowledge gaps
in the potential for producing biomass and lipids from algae biolm growth systems.
& 2015 Elsevier Ltd. All rights reserved.
Keywords:
Microalgae
Biolm
Biofuels
Lipids
Growth parameters
Productivity
Contents
1.
2.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 418
Composition and structure of an algal biolm. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 419
2.1.
Extracellular polymeric substances and matrices. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 419
2.2.
Species and succession of photosynthetic biolms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 420
3. Algae biolm biomass and lipid production. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 421
3.1.
Algae biolm attachment to growth materials. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 421
3.1.1.
The affect of material properties on algae biolm growth . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 421
3.1.2.
Biotic factors on biolm development and growth . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 422
3.2.
Key growth parameters and their affect on algae biolm biomass productivities . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 423
3.2.1.
Light intensity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 423
3.2.2.
Carbon dioxide concentrations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 424
3.2.3.
Other growth factors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 424
3.3.
Algae biolm biomass lipid potential . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 425
3.3.1.
Lipids and lipid concentration enhancement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 425
3.3.2.
Algae biolm productivities . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 426
4. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 426
Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 427
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 427
1. Introduction
Corresponding author. Tel.: 1 416 978 8517.

E-mail addresses: Peter.schnurr@utoronto.ca (P.J. Schnurr),
Dgrant.allen@utoronto.ca (D.G. Allen).
http://dx.doi.org/10.1016/j.rser.2015.07.090
1364-0321/& 2015 Elsevier Ltd. All rights reserved.
Algae growth systems show great potential for the production

of biofuels and bioproducts. The main reasons for this are due to
their high growth rates doubling times as low as 78 h [1] and
P.J. Schnurr, D.G. Allen / Renewable and Sustainable Energy Reviews 52 (2015) 418429
high concentrations of valuable biocompounds. Coupled together,

high biomass growth rates and biocompound concentrations
results in high overall productivities of valuable biocompounds.
For instance, Mata et al. [2] estimated that microalgae could
generate between 58,700 and 136,900 L/ha yr of biodiesel
depending on biomass lipid contents of 30% or 70% compared
to 5366 L/ha yr for the best terrestrial biodiesel crop (Palm Oil).
Other valuable biocompounds of interest within algae biomass are
amino acids, fatty acids, pigments, carbohydrates, polysaccharides,
vitamins, and antioxidants, which can be used to generate nutraceuticals, pharmaeucticals, functional foods and food additives,
farm and aquaculture feed, biofuels, cosmetics and bioplastics
[24]. In addition to high productivities, growing algae has
advantages over conventional biofuel sources because it can be
grown on non-arable lands, growth ponds and reactors can be
scaled vertically, and algae can be grown on wastewater [57] and
ue gas waste streams [8,9], thereby providing essential nutrients
for growth to the algae while simultaneously mitigating pollution
from these waste streams.
Researchers have identied several key limitations to commercialization of biofuels and bioproducts from algae growth systems,
including optimizing growth rates and internal biochemical compositions through genetic modication of species, optimization of
growth conditions and reactor design, and developing the biorenery
concept for algae [10]. Many researchers agree that one of the most
signicant economic limitations to commercialization, however, is
the harvesting and dewatering of algae biomass grown planktonically
estimated to be up to 30% of the production costs [1113]. By
growing algae as a biolm there is potential to signicantly reduce
these costs because the biomass is immobilized and much more
concentrated 0.4% (g/g) for planktonic systems [10], compared to
816% in biolms [14,15]. The immobilized nature may also make
downstream processing easier and more economical.
There has, however, been a limited amount of work conducted
on the production of biofuels and biochemicals with algae biolms
compared to planktonic growth systems. Of the work that has been
done on algae biolms for biofuel production, much of it revolves
around the study of the attachment, and subsequent growth, of
algae biolms to various growth materials [14,1623]. There has
also recently been a signicant amount of algae biolm research on
novel reactor designs studying biomass and lipid production rates
[14,1718,20,21,2429]. Other studies on algae biolms have related
not specically to biofuel and bioproduct production, but rather, on
using them to treat wastewaters of nitrogen and phosphorus using
algal turf scrubbers and novel biolm growth systems [56,3038].
Additionally, there are many studies on algae biolms from a
fundamental perspective i.e. oxygen proles under various conditions, species composition and succession, affects of shear rate,
affects of temperature, etc., which is helpful in understanding how
to optimize growth rates and lipid concentrations for biofuel and
biochemical production. Lastly, there is a large breadth of knowledge on bacteria biolms and planktonic algae growth systems that
may provide insights into algal biolm systems.
This review paper summarizes the current knowledge of algae
biolms, and how it relates to the production of biomass and
biofuels. The overall objective of this paper is to provide an overview for what we currently know about algae biolm development
and composition, and growth parameters that affect growth rates
and internal biomass lipid concentrations. The review will include
studies done on algae biolms for biofuel and biochemical production, on algae biolms studied from a fundamental perspective, and
on algae biolms used to treat wastewater streams. It will also draw
from the extensive literature on bacterial biolms and planktonic
algae growth systems to make inferences about algae biolm
growth systems. This review will not focus on reactor design, since
reactor designs were covered extensively by Berner et al. [39]. A
419
review such as this is important as algae biolm biofuel and

biochemical growth systems have emerged as a promising biotechnology over the past 5 years, evidenced by the growing number of
groups working on such systems. To the best of our knowledge no
such review has been written to date.
2. Composition and structure of an algal biolm

Biolms are communities of microorganisms attached to each
other and a solid growth substratum. They form virtually anywhere water exists for extended periods of time. Photosynthetic
biolms in nature are often referred to as periphytic or algae
biolms, which are mostly composed of algae, cyanobacteria, and
heterotrophic bacteria living in symbiosis. The composition and
structure of photosynthetic biolms will vary according to abiotic
and biotic factors within the environment.
2.1. Extracellular polymeric substances and matrices

In biolms, extracellular polymeric substances (EPS) are biomolecules and inert solids that bind cells to each other and to solid
materials. Extracellular polymeric substances are located on the
outside of cells, generated through active secretion, cell lysis,
shedding of cell surface material, and adsorption from the environment [40,41]. The predominant EPS are polysaccharides and
proteins; however, nucleic acids, lipids, and suspended solids can
also make up the EPS matrix [42].
In well-developed biolms the EPS forms a matrix that creates a
microenvironment for the cells. This microenvironment protects cells
from environmental stress such as dehydration, and uctuations of
pH, temperature, and nutrient concentrations [41,43,44]. Additionally,
EPS matrices are known to act as a nutrient reservoir as enzymes
within the matrix digest EPS and inert solids, [45], and the EPS acts as
an ion exchange resin as it traps nutrients through sorption [40,46]. In
these ways the EPS matrix helps accumulate and concentrate
nutrients from the bulk medium. Although EPS is 99% water and
collapses upon itself when dehydrated [47], it can compose up to 90%
of the organic matter in some (bacterial) biolms [46].
During biolm formation and growth, microalgae will respond
to environmental circumstances by increasing or decreasing the
expression of specic promoters that affect EPS production. For
instance, Becker [48] demonstrated that the diatom Amphora
coffaeformis increases EPS production when it is in contact with
materials that have good adhesion strength with EPS. A growth
material effect on algae EPS production was also demonstrated by
Shen et al. [28]. Additionally, Domozych [49] and Shen et al. [28]
demonstrated that increasing nutrient concentrations, particularly
nitrogen, would increase EPS production from diatom and green
algae species. This is likely because a signicant fraction of EPS is
composed of proteins [28], allowing the cells to over-produce
amino acids while nitrogen is abundant and environmental conditions are favorable. There is some evidence that suggests algae cells
increase their EPS production as their colonies age and mature
[28,48]. This could be a result of mature colonies allocating less
resources into reproduction i.e. reaching a stationary growth phase,
and more into stabilizing their biolm community. Lastly, there is
evidence that temperature stress and mineral (calcium) accumulation stress adversely affect EPS production from algal cells [49].
Although it is clear that algae cells produce EPS according to
environmental stimuli, compared to bacterial systems, the literature
on EPS production and EPS matrices in axenic and mixed community algal biolms is limited. This is an opportunity for fundamental
algal biolm knowledge development.
420
Fig. 1. Development of a mixed community algal biolm: (A) growth surfaces are rst conditioned with bacteria cells that excrete the initial EPS matrix; (B) various species
of algae cells present in the bulk medium then begin to colonize the EPS matrix; (C) the algae cells grow and reproduce, forming a symbiotic relationship with the bacteria
present in the EPS matrix; and (D) a mature biolm matrix is densely populated with algae cells, particularly cyanobacteria and chlorophytes, and retains nutrients in the EPS
matrix.
2.2. Species and succession of photosynthetic biolms

Photosynthetic biolms have many different algae, bacteria,
cyanobacteria, protozoa, and multicellular microorganism species
present within them. Diatoms, green algae, and lamentous algae
are groups of algae that usually compose signicant fractions of
biolm biomass; some of these species are known to grow both
autotrophically and heterotrophically [50,51]. Bacteria species within
biolms include cyanobacteria, and heterotrophic and autotrophic
bacteria. Organisms within biolms form symbiotic relationships
with one another, whereby heterotrophic bacteria supply carbon
dioxide during respiration, and photosynthetic organisms utilize the
carbon dioxide to generate biomass, thus producing the oxygen for
bacteria during respiration [5255]. Additionally, carbohydrates,
vitamins and organic compounds are excreted by, and become
nutrients for, both algae and bacteria within the biolm [52]. Mature
biolms reach a steady state with organisms within the biolms and
the environment in which it exists.
Biolm maturity affects the succession of species present i.e.
abundance and proportions of algae, bacteria and EPS (Fig. 1). Early
stage development photosynthetic biolms have a high proportion
of EPS and bacteria compared to algae and cyanobacteria [56,57].
Some researchers refer to this as conditioning of the biolm
growth surface (Fig. 1A). Mack and Anderson [58] reported that,
after the establishment of the EPS matrix, algae cells begin to
rapidly grow in the upper layers (Fig. 1B and C) of the matrix
causing bacteria to form aerial colonies (away from the substrate) to
compete for nutrients. If the environmental conditions are favorable
(discussed later), a mature algae biolm will form, consisting of a
dense and diverse population dominated by algae cells (Fig. 1D)
[56,57,59]. The biolm matrix facilitates the retainment and sharing
of nutrients, as symbiotic relationships exist between the heterotrophic and autotrophic microorganisms (Fig. 1C and D).
Biolm maturity also affects the succession and proportions of
specic algal groups. Researchers have demonstrated that diatoms
make up a signicant fraction of early biolms i.e. rst 1520 days of
growth, while lamentous chlorophytes become predominant afterwards [60,61]. However, Sekar [62] reported that early phase biolm
succession (14 days) is dominated by green algae, followed by a
second phase (59 days) dominated by diatoms, and lastly, a third
phase dominated by cyanobacteria (1015 days). Zippel and Neu [57]
also demonstrated that cyanobacteria are a late successional microorganism. The differences of succession of algae species is likely
attributed to the types of species initially present in the growth
medium, and how they respond to the particular abiotic growth

conditions of the experiment. The literature suggests that non-axenic
photosynthetic biolms eventually become dominated by chlorophytes (single celled and lamentous) and cyanobacteria given enough
time, and provided any form of seeding mechanism. This has
implications for long-term operation of algae biolm growth systems,
as species type has signicant potential to affect overall biomass and
lipid productivities, as will be demonstrated later in this paper.
Nutrient concentrations and light intensity have a strong effect
on the abundance of algal species in a biolm, compared to
heterotrophic bacteria, EPS and inert solids. Organic and inorganic
carbon concentrations in the growth medium will affect the
abundance and proportions of algae compared to bacteria high
inorganic and low organic carbon results in algae dominated
cultures [55]. In addition to carbon species concentrations, Villanueva et al. [63] and Kebede-Westhead et al. [35] demonstrated
that increases in nitrogen and phosphorus loading rates cause
signicantly greater photosynthetic biomass accumulation compared to bacteria. With adequate nutrients and light, photosynthetic
biolms will be greater than 75% algae biomass [56,57]; however,
when biolms become too thick, or light intensities insufcient,
light limitation will occur and the biolm layer furthest from the
light source (light limited) may become dominated by bacteria, EPS,
and other non-photoautotrophic materials, as was demonstrated by
Kuhl et al. [64] and Guariento et al. [65]. Fig. 2 demonstrates these
photosynthetically inactive layers and their respective depths
under different light regimes increased light intensity increases
the photosynthetically active regions of the biolm, and the overall
amount and proportions of algae biomass. This idea is discussed
later in the light intensity section of this paper.
Light intensity, temperature, nutrient concentrations, and shear
rates affect the succession of photosynthetic biolms in terms of
what algal species are predominant. Congestri et al. [59] and Davies
et al. [66] concluded that seasonal light and temperature uctuations in wastewater treatment plants affected the proportions of
specic algal groups/species in biolms. More specically, KebedeWesthead et al. [35] reported that diatoms were more prominent
under low light conditions (270 mol/m2/s) compared to high light
conditions (390 mol/m2/s), and Villanueva et al. [63] reported that
diatoms were a major biomass fraction in lower temperatures (7
11 1C) conditions compared to higher (1115 1C) temperature.
Moreover, cyanobacteria proportions were shown to increase relative to the diatom and green algae populations when temperatures
were increased from 12, 18 and 24 1C [67]. This is not surprising as
Low Light
Intensity
Photosynthetically
Active Region
Growth Material
High Light
Intensity
Growth Material
Medium Light
Intensity
Photosynthetically
Active Region
Photosynthetically
Inactive Region
Photosynthetically
Inactive Region
Growth Material
Photosynthetically
Active Region
421
Photosynthetically
Inactive Region
Fig. 2. Schematic of light proles through an algae biolm at various light intensities: photon penetration through algae biolms increases with increasing photon ux
density. Thick algae biolms have relatively thin photosynthetically active regions adjacent to their source of light, but comparatively thick photosynthetically inactive
regions opposite the light source (A); as light intensity increases the photosynthetically active region increases due to increased photon penetration, and the subsequent
reduction of antennae size/number within this regions (B) and (C).
cyanobacteria is known to thrive under higher temperatures

optimal temperature between 30 and 35 1C for Aphanothece microscopica Nagali and Spirulina platensis grown planktonically [68,69].
Increased loading rates of nitrogen and phosphorus also seem to
favor cyanobacteria, composing up to 65% of the biolm under
these conditions [63]. Besemer et al. [60] reported the affects of
ow regime on succession. Particularly, it was shown that coccal
chlorophytes were more abundant under laminar and transitional
ow than in turbulent ow, and that operational taxonomic units
(number of species) decreased as ows were increased.
Biolm succession is extremely complicated, but is clearly
affected by biotic factors i.e. the types of species present, and
abiotic factors of the growth environment. It appears that high
nitrogen and phosphorus loadings, inorganic carbon concentrations,
and light intensities increase photosynthetic biomass accumulation
and proportions compared to non-photosynthetic biomass. Additionally, matured cultures, and high temperature and nutrient
loading rates cause signicant increases in cyanobacteria proportions in photosynthetic biolms. Because some species present in
photosynthetic biolms produce signicantly less lipids and other
valuable compounds, it is important to know how biotic and abiotic
conditions affect the proportions and abundances of these species.
Future studies might consider studying (long-term) succession of
algae biolms to control for high proportions of high productivity
species both in terms of biomass productivities and of lipid and
other high value product biomass concentrations.
3. Algae biolm biomass and lipid production

Compared to planktonic algae growth systems, there has been a
limited amount of work on algal biolm growth systems for the
production of biofuels and biochemicals. Of the algal biolm
biofuel research conducted to date, many researchers have focused
on the affects of growth materials on biolm attachment and
biomass accumulation [14,1623], and on novel reactor designs
and the biomass and lipid productivities they can produce
[14,17,18,20,21,2429]. Additionally, there has been some work
on how different growth parameters e.g. light intensity
[18,26,35,70], CO2 concentrations [26,29,71], etc., affects biomass
accumulation, and on quantifying and manipulating biomass lipid
concentrations [2427,72,73]. Additionally, much research has
been done from a fundamental understanding of algae biolms
in nature [57,63,64,74,75], and in using biolms to treat wastewater of contaminants [5,6,3038]. The section below draws on
these studies, and on the extensive amount of literature on
planktonic algae growth, to determine how to potentially maximize productivity of algae biolm growth systems.
3.1. Algae biolm attachment to growth materials
Because biolms, by nature, are attached to a solid (growth)
material, it is important to understand if material properties affect
biolm formation, growth, and development. Growth material
properties studied by researchers are surface tension/surface wettability/water contact angle/hydrophobicity, polar surface energies,
and surface micropatterning. In addition to material properties, cell
recruitment and overall biolm growth is a result of biotic factors
such as the presence of rst inhabitors and extracellular polymeric
substances [53,56,58,76], and the re-growth of biolms already
acclimated and succeeded to the growth conditions [14,18,20].
3.1.1. The affect of material properties on algae biolm growth
Some researchers have studied differences in biolm growth
with different materials without quantifying the material properties, and found there are differences in growth rates. For instance,
Johnson and Wen [20] studied biolm growth rates on polystyrene
foam, cardboard, polyethylene fabric, and loofah sponge. They
found that polystyrene foam yielded signicantly higher biomass
productivities than the other materials tested, but gave no potential reason for this higher yield. Similarly, Christenson and Sims
[14] and Gross et al. [18] found that cotton rope and cotton duct,
respectively, were the best materials they each tested for growth.
It is clear different materials do affect biolm growth and development, but understanding the properties of these materials is
critical to understand and predict biolm formation and growth.
Research conducted on the affects of material properties on algal
biolm growth is somewhat inconclusive. Some researchers have
demonstrated a correlation between hydrophobic surfaces and
biolm formation and growth. Specically, they conclude that
hydrophobic surfaces are ideal for the growth of biolms
[16,22,77]. The theory behind the affects of hydrophobicity is that
hydrophobic molecules, particles, and cells, prefer a hydrophobic
environment, and will therefore adhere to each other to minimize
their contact with water [78]. Other researchers, on the other hand,
found no correlation or weak correlations between hydrophobicity
and algal biolm formation and growth [17,19]. The difference
between these groups of researchers and their ndings is the length
of the growth period and the density of the biolm grown.
Researchers reporting an affect of material properties on growth
did not observe growth over the long-term i.e. they observed initial
422
recruitment to the growth material; however, the groups reporting

no effect grew thick biolms for relatively long periods of time i.e.
the cells were eventually growing on top of each other. Genin et al.
[17] attributed differences in overall algal biolm productivity to
differences in colonization time, and that that colonization time i.e.
recruitment, is highly correlated to polar surface energies of growth
materials. Corresponding to the above conclusions, Ozkan and
Berberoglu [22] reported differences in cell attachment between
diatoms and green algae according to the hydrophobicity of the
surface, and that hydrophobic cells adhered to hydrophobic surfaces
more strongly than hydrophilic cells did to hydrophobic and hydrophilic surfaces. They also concluded that, above all else, acidbase
interactions were the dominating mechanism for cell attachment to
substrata and each other. From the research on material properties it
would appear that polar surface energies, and cellcell and cell
substrata hydrophobicity and acidbase interactions are important
parameters to consider for biolm formation and short-term growth.
Once cells have adhered to a subsurface and conuence is reached,
however, cells are growing on top of each other and long-term
biolm biomass growth is a function of other growth parameters i.e.
nutrient concentrations, light availability, etc.
Surface roughness and micropatterns affect cell recruitment and
short-term biolm biomass accumulation rates, but not long-term
growth trends. A preliminary study conducted by Cao et al. [79]
showed algae cell populations were enhanced by micropatterning
stainless steel growing surfaces. Similarly, Sekar et al. [77] demonstrated more biolm cell attachment with increasing surface roughness of algae grown on both titanium and stainless steel growth
substratum. In both of the above studies it is important to consider
that the differences observed were after short growth periods and
low population densities i.e. attachment and recruitment rather
than growth. It is likely that surface roughness differences do not
actually affect overall biolm productivity rates over long term
growth periods when cell densities are high i.e. after cell conuence
is reached. This was demonstrated by Irving and Allen [19] and
Blanken et al. [71] as they concluded no statistically signicant
long-term algae biolm productivity gains from patterning the
surface. Their data does also, however, suggest signicant shortterm gains (rst 23 days of growth) from micropatterned surfaces.
Micropattern dimension and depth, compared to cell size, may be
a signicant factor in micropatterning over short-term growth
periods. Sathananthan et al. [23] tested 3 different micropatterns
on algal biolms grown for 10 days and did not observe increased
growth (compared to smooth surfaces) in shallow (1.5 m
deep 20 m wide) horizontal and vertical grooved surfaces. They
did, however, see signicant gains in biomass productivity with deep
and wide (20 m deep 20 m wide) v-groove shaped micropatterns. They attributed the negative growth results on the horizontal
and vertical micropatterns, compared to the v-groove surfaces, to cell
size (10 m) vs. groove depth ratios i.e. the horizontal and vertical
micropatterns were not deep and wide enough for the cells to t
within. The discrepancy in the effects of micropatterned surfaces
across long and short-term growth periods is likely a result of cell
recruitment and conuence, as was described above and by Genin
et al. [17]. On micropatterned surfaces it is likely that surface
roughness affects early biolm growth rates through recruitment
and colonization, but once conuence is reached, the patterning does
not affect the biolm biomass growth and accumulation.
Although material properties do not seem to affect overall
long-term algae biolm biomass productivities, it is possible that
these material properties affect biolm adhesion strength e.g.
resistance to shear stress as crevices act as anchor points sheltered
from shear stresses, or intermolecular interactions between cells
and surfaces. This is a potentially important topic for future algae
biolm biofuel studies. Additionally, it is possible that growth
material properties may also affect the types of cells that are
recruited to the substratum (e.g. cell size to groove size ratios), and
the subsequent succession of the culture.
3.1.2. Biotic factors on biolm development and growth

In addition to material properties, algae biolm formation and
growth is a result of surfaces conditioned with extracellular polymeric substances (EPS) from algae and bacteria. This occurs as
molecules accumulate at the solid-liquid interface of surfaces causing
an increase of nutrients, adsorption of proteins and other EPS, and a
gradual change in physical-chemical properties of the surface i.e. free
surface energy, hydrophobicity, electrostatic charges, etc. [78]. Generally, the rst inhabitors of algal biolms are bacteria that begin to
form an EPS matrix while cells begin to grow away from the growth
surface [56,58]. After this conditioning has occurred algae cells are
recruited to the matrix and grow in symbiosis and in competition
with the bacterial cells present [55,58].
Many researchers have demonstrated that the presence of bacteria, and the resulting symbiotic relationships, is highly benecial
for the recruitment and overall growth of algal biolms [19,53,62,76].
This was demonstrated by Hodoki [53], who showed signicant
increases in biolm-chlorophyll concentrations (algal biomass) with
increasing pre-conditioned bacterial biolm concentrations. Additionally, Hodoki [53] demonstrated that the addition of algae caused
an increase in bacterial biolm populations, supporting the idea of
symbiotic relationships in mixed community biolms. In his study,
Holmes [76] found a 12 orders of magnitude increase in biolmchlorophyll in bacteria-associated experiments compared to axenic
algae biolm cultures. Lastly, Irving and Allen [19] demonstrated a 9fold increase in algae biolm thickness when grown on non-sterile
secondary wastewater efuent, compared to sterile wastewater. They
also demonstrated that in unsterile wastewater, algae cells had a
propensity to switch from planktonic to sessile state, and had a much
greater resistance to shear stress. The researchers concluded that all
of these phenomena were a result of the bacteria and EPS present in
the unsterile wastewater medium, which are not normally present in
standard (sterile) growth medium. Surface conditioning with
microbes and EPS is important for early stage algal cell recruitment,
but because of the requirement for EPS in biolm growth and
stability, EPS producing microbes are likely advantageous for longterm growth and resistance to shear stress as well. It is currently
unclear whether axenic algal biolms outperform the mixed community algal biolms described above in terms of growth rates,
maximum thickness, lipid production, resistance to shear stress, etc.,
and is therefore an opportunity for future research.
Re-growing a partially harvested biolm has signicant growth
rate advantages compared to growing a biolm from a clean
surface. With their Rotating Algal Biolm Reactor (RABR), Christenson and Sims [14] produced a signicantly higher biomass productivity when re-growing partially harvested biolms compared to
biolms initially grown on a clean surface 5.5 g/m2/d compared to
2.6 g/m2/d, respectively. Gross et al. [18] and Johnson and Wen [20]
also demonstrated signicant increases in biomass yields and
productivities when re-growing a partially harvested biolm compared to one initially grown on a clean surface. The observed
increased biomass productivities from re-growing a partially harvested biolm are likely a result of two things: (1) the growth
material is already pre-conditioned with residual EPS, and bacterial
and algae biomass, eliminating the lag phase of cell recruitment;
(2) and the microbes present in the residual biomass culture are
already acclimated to the environmental growth conditions and in
symbiosis with each other. By micropatterning growth materials, it
may be possible to provide a sheltered habitat for a fraction of the
biolm and cells during the harvesting processes. In such a scenario
a small proportion of the already acclimated biomass may remain in
the crevices to re-grow into a thick biolm again.
3.2. Key growth parameters and their affect on algae biolm biomass
productivities
The economic viability of biofuel and bioproduct systems from
algae biolms will largely depend upon biomass rates of production. There are several key growth factors that signicantly affect
the growth rates of algal biolm biomass. These main growth
factors, outlined below, have been identied from the signicant
quantity of work already conducted on planktonic algae growth
systems for biofuel and bioproduct production, the somewhat
limited work on algae biolm systems, and what is known about
how algae biolms grow in nature.
3.2.1. Light intensity
Light intensity is an important growth parameter that signicantly affects algae growth kinetics of both planktonic and biolm
cultures. Many planktonic algae researchers have shown that growth
rates are signicantly increased with increasing photon ux density
(PFD); however, once the point of light saturation is reached and
surpassed i.e. the PFD is too high, photoinhibition and photooxidation can occur causing cultures to cease to grow, or even die [8085].
To some extent algal cells in planktonic and biolm systems can
acclimate to high and low light intensities by producing a proportional amount and size of photosynthetic reaction center antennae
complexes to efciently harvest and utilize the available photons of
light [8689]. By doing this, algal cells that were once photo-limited/
inhibited can begin to grow and thrive under low/high light conditions. Additionally, smaller and fewer antennae allow more light to
transmit through algae cells to other cells that would otherwise be
shaded. These phenomena are particularly relevant for algae biolms because cells are immobilized and orders of magnitude more
concentrated than planktonic growth systems.
Like planktonic algal systems, algal biolm growth rates appear
to be correlated to the light intensities irradiating them; however,
light intensity proles and their relationship to growth are much
more complicated for biolms than for planktonic systems. For
instance, Liu et al. [26] demonstrated that biomass productivity
increased linearly from 0.7 to 10 g/m2/d when light intensities were
increased from 0 to 150 mol/m2/s, but there was a slight diminishment on return of PFD input when light intensities of 150
300 mol/m2/s were tested. The authors concluded that the reason
for these diminishing returns was because the light saturation point
(LSP) was reached, but LSP is complicated for algal biolm systems
because of their highly concentrated and immobilized nature
(compared to well mixed planktonic systems). For instance, the
LSP may have been reached where the biolm surface is being
irradiated from, but light is attenuated exponentially through a
423
biolm [56,61], so depending on its thickness, a large proportion of

the biolm could be light limited/photosynthetically inactive
(Fig. 2). Schnurr et al. [15] demonstrated these types of light
limitations whereby cells adjacent to the light source were receiving
high PFD's, but cells 150 m into the biolm and greater were in
near dark conditions due to light attenuation. Additionally, light
limitations in biolms were indirectly demonstrated by Dodds et al.
[74], Kuhl et al. [64] and Jensen and Revsbech [75], who reported
various oxygen proles in photosynthetic biolms irradiated with a
range of light intensities. In these studies, relatively high oxygen
concentrations were observed in the portion of the biolm nearest
to the light source, with much lower oxygen concentrations further
from the light source. Furthermore, the oxygen concentrations were
higher, and were higher at greater depths, when the biolms were
irradiated with higher light intensities. The work above suggests
that photon penetration through a biolm is related to the light
intensity irradiating the biolm. Because of this, thick algal biolms
have a photosynthetically active region adjacent to the light source,
and the depth of that photosynthetically active region is related to
the light intensity irradiating the biolms (Fig. 2). It is plausible to
conclude that the more photosynthetically active an algae biolm is,
the higher the biomass productivities.
To maximize productivities, it would be ideal to maximize
photon penetration into a biolm while limiting photoinhibition,
photoxidation, and (photo)acclimation. A way to potentially do
this is to irradiate the biolms with optimal light intensities from
both directions i.e. the materials side and the water-side. Schnurr
et al. [15] demonstrated this concept, but because the total PFD
was kept constant when testing individual sides compared to both
sides i.e. 100 mol/m2/s from one side or 50 mol/m2/s from each
of the two sides, they reported no signicant difference in algal
biolm growth when irradiating from both sides. By having the
optimal light intensity irradiate the biolms from both sides,
photon penetration, and hence biomass productivity, could be
maximized. The effects of light direction (into an algae biolm) at
various light intensities could provide valuable insight into maximum photon penetration into a biolm, and hence maximum
growth rates and thicknesses.
Some studies have shown increases in algae biolm biomass
productivities with increased PFD's. For instance, Craggs et al. [5]
and Gross et al. [18] both reported signicantly higher biolm
biomass productivities in the summer than in the winter. The
increased productivities were mainly attributed to increased PFD's
and temperatures in the summertime, but due to varying daily
temperatures, PFD's, and lengths of photoperiods, it's not possible
to separate the effects. Kebede-Westhead et al. [35] reported
biolm biomass productivities of 14.8 and 17.2 g/m2/d at 270 and
Table 1
Comparing algae biolm biomass productivities from different studies with different light intensities.
Light Intensity
(lmol/m2/s)
Productivities
(g/m2/d)
Photoperiod
(h/d)
Carbon dioxide
(%)
Temperature
Species
Reactor type
Reference
2242
55
30220
100
110120
40140
160
170
261
270
300
390
642
422
1
0.71
1.3
6.5
2.6
5.35.5
2.8
2.5
2
14.8
15
17.2
4.3
17.520.1
Summer average
24
Summer average
Not available
Not available
16
16
14
Winter average
23
24
23
Summer average
24
0.04
0.04
0.04
1
0.04
0.04
2
0.04a
0.04a
0.04
2
0.04
0.04a
N/A
1832
N/A
1832
25
20
22
25
1424
N/A
1924
30
1924
N/A
38
Halochlorella rubescens
Botryococcus braunii
Halochlorella rubescens
Botryococcus braunii
Chlorella sp.
Mixed consortia
Nitzhia palea
Diatoma, Pediastrum, Chlorella
Chlorella vulgaris
Mixed lamentous dominated
Scenedesmus obliquus
Mixed lamentous dominated
Chlorella vulgaris
Chlorella sorokiniana
Vertical at plate PBR

Horizontal at plate PBR
Rotating algal biolm reactor
Algal turf scrubber
Algal turf scrubber
Rotating biological contactor
[36]
[21]
[36]
[27]
[20]
[38]
[24]
[14]
[18]
[35]
[26]
[35]
[18]
[71]
Denotes carbon dioxide concentration that was exposed to biolms through air, rather than bulk liquid growth medium.
424
390 mol/m2/s in an algal turf scrubber under controlled conditions demonstrating the potential of increased PFD's. Similarly,
Naumann et al. [70] used a range of low light intensities to
demonstrate increases in biomass productivities with increase
PFD's with various algal species grown.
Comparing reported biolm biomass productivities and the light
intensities irradiating them from various studies also reveals some
correlations between growth rates and light (Table 1), but the trend
is much less clear because of a lack of controlled variables between
the experiments. These important controlled variables for algae
biolm systems are the: (1) photoperiods irradiating the biolms;
(2) photobioreactor designs and hence their shear stresses, hydraulic and solids retention times, etc.; (3) species used and how well
acclimated they are to the environmental conditions; (4) temperature of the growth medium; (5) nutrient loading rates/concentrations; (6) carbon dioxide concentrations; (7) and pH of the growth
medium. Many of the above variables reported in Table 1 are likely
to contribute to the high variability of reported biolm biomass
productivities. In order to properly access the effects of light
intensity on algal biolm growth, a large range of PFDs irradiating
the biolms should be tested while controlling all of the above
growth parameters. Lastly, the range should go up to, and potentially beyond, the light intensities that resemble summertime sunlight conditions i.e. 2500 mol/m2/s of photosynthetically active
radiation (400700 nm wavelength).
3.2.2. Carbon dioxide concentrations

Like light intensity, carbon dioxide (CO2) concentration is a
parameter that signicantly affects algae growth kinetics. However, although there have been many researchers who have
studied the effects of carbon dioxide concentration on planktonic
algae growth, there has been a limited amount on algae biolm
growth. For most algal species grown planktonically, increasing
the CO2 concentration (to 57% (v/v)) signicantly increases
growth rates, until the concentration becomes too high and
negatively affects growth [8,9093]. It is very probable that a
similar phenomenon exists with algal biolms. Since algae biolms are very dense at approximately 816 g/L [14,15], it is likely
that high CO2 concentrations will be useful for mass transport
across the lm, and hence, better growth kinetics.
Current work on algal biolm growth relating to carbon dioxide
concentrations is inconclusive. Gross et al. [18] created a reactor that
allowed for control of the gaseous phase CO2 concentration that was
directly exposed to algae biolms for extended periods of time. They
reported that incrementally increasing gaseous phase CO2 concentrations from atmospheric to 3% did not produce increase yield or
productivity of algal biolms. On the other hand, Blanken et al. [71]
and Kessano et al. [29] dissolved the inorganic carbon directly into
the growth medium in which the algae biolms were grown. The
former research group observed signicant increases in biomass
growth rates when concentrations were increased incrementally,
while the latter did not observe a signicant increase in growth
when raising concentrations 2.5-fold. The differences in growth
response to dissolved inorganic carbon concentrations may be
explained by the differences in light intensities irradiating the
biolms i.e. an interaction effect between CO2 and light. Each of
the two experiments that did not produce a response to increased
CO2 concentrations had low light intensities (110120 and 227 mol/
m2/s) irradiating the biolms compared to the study that had a
growth response (422 mol/m2/s). In the event that there is an
interaction effect, it is possible that biolms not observing an effect of
CO2 did not have enough photons to assimilate the excess carbon.
Comparatively, in the Blanken et al. [71] study, the high PFD may
have allowed the differences in CO2 to be pronounced in the form of
carbon assimilation and biomass production. Lastly, it is also possible
that reactor design played a role in the observed effect. Both studies
that did not observe a growth rate increase with increased CO2 used
similar rotating algal biolm reactors (RABR), while the Blanken et al.
[71] study used a rotating biological contactor that yielded extraordinarily high productivities. It is possible that the different reactors
facilitated different mass transport effects i.e. biolms exposed to CO2
in air compared to water, causing carbon saturation even at the
lowest CO2 concentrations for the RABRs.
There are a number of studies on modeling inorganic carbon
species, and their respective concentrations and ux behaviors in algal
biolms. Of this work, researchers show that, as dissolved CO2 (dCO2)
concentrations rapidly decrease (to trace concentrations) across a
biolm due to boundary layers [94] and utilization by algae, pH
rapidly rises to very basic conditions i.e. pH 1012, causing an
equilibrium shift towards bicarbonate and then carbonate ions
[9496]. Although some literature suggests that algae can use bicarbonate as an inorganic carbon source [97], most researchers state that
the more easily used form of inorganic carbon is dCO2. According to
models, the predicted pH and inorganic carbon species concentrations
in thick algal biolms renders them dCO2 limited [94,95], but that is
with low (near atmospheric partial pressures) bulk medium concentrations of carbon dioxide. Models suggest that these limitations can
be reduced, to some extent, by decreasing boundary layer thicknesses
through increased ow rates [94], and by increasing inorganic carbon
ux by increasing alkalinity, phosphate buffer concentrations, bulk
medium dCO2 concentrations, and light penetration deeper into a
biolm via higher light intensities [95,96,98].
Future experimental work on the effects of CO2 concentration on
algae biolm growth should focus on testing various CO2 concentrations with different reactor types. These studies should also
consider the various effects of mass transport and interacting
chemical species/phenomena on overall biolm biomass productivity. As mentioned above, models predict that dCO2 mass transport
into biolms is signicantly enhanced when the pH in the biolm is
kept near neutral, and this can be done when the bulk medium has
an increase in dCO2 concentrations, (phosphate) buffer concentrations, and alkalinity. Additionally, increased bulk medium ow rate
across algal biolms decreases boundary layer length and increases
dCO2 mass transport [94]. The above experimental work should
consider all of these parameters when attempting to understand
algae biolm growth as it relates to inorganic CO2 concentrations.
3.2.3. Other growth factors

Other factors that are known to signicantly affect algae growth,
but have not been thoroughly studied for algae biolm systems are
temperature, pH, macronutrient concentrations, and shear stress.
The optimal temperature for algae growth (planktonically and in
biolms) is dependent on the species present in the community and
interacting variables such as light intensity [81,99]; however, a
typical optimal temperature range for algae growth for many
species is approximately 25 1C [81,99101]. More work studying a
range of temperatures, and potentially interacting variables, on
algae biolm growth would be useful. As discussed above, dCO2
utilization by algae, and concentrations of alkaline minerals and
phosphate buffers, signicantly affects pH within a biolm, and the
pH affects the species of inorganic carbon present in the medium
and within the biolm. Since dCO2 is considered the most usable
form of inorganic carbon for algae, and since near neutral pH
maximizes dCO2 concentrations at equilibrium without causing
detrimental acidic environments, a near neutral pH should yield
the best growth results for algal biolms. There is opportunity for
algae biolm researchers to explore these pH phenomena, and their
effects on algae biolm growth. Increasing macronutrient (nitrogen
and phosphorus) concentrations and reactor loading rates have
been shown to signicantly enhance algae biolm biomass
accumulation and overall growth rates [31,35,63], but these growth

rates can peak at milli mole nitrogen levels [25], and can even
become detrimental to growth rates at excessive loading rates [31].
There is opportunity to further our knowledge in this eld of algae
biolm growth, particularly relating to excessive nutrient loading.
Lastly, shear stress is known to facilitate the adhesion of cells to
form biolms [102]; however, shear stress increases, at some point,
become detrimental to biolm formation, development, growth
and adhesion. Although Besemer et al. [60] briey investigated ow
regimes on biolm growth, to our knowledge no researcher has
thoroughly studied a broad range of dened shear stresses on algae
biolm growth and succession; this is another opportunity for
future work on algae biolm growth systems.
Algae biolm growth will, to a great extent, be affected by all of
the growth parameters described above. Photobioreactor design
may also yield unique results from each growth parameter e.g. CO2
delivery in air compared to water, shear rates and the effect on mass
transport/boundary layers, etc. Generally, increasing the magnitude
of these parameters (with the exception of pH) will positively affect
algae biolm growth until, at some point, increasing the magnitude
becomes detrimental to biolm biomass productivity. The focus of
future algae biolm biochemical researchers should be to determine where that maximum productivity resides for each growth
parameter, including interacting parameters.
3.3. Algae biolm biomass lipid potential
In addition to biomass growth rates, another critical factor in
biolm biofuel and biochemical economics is the concentrations of
valuable compounds within the biomass, as that signicantly
affects overall biochemical productivity. Currently, the main algae
bioproducts of interest are lipids, proteins, carbohydrates, various
nutraceutical compounds, and the residual biomass (post extraction) for anaerobic digestion; however, the scope of this review
only covers algae biolm lipids, since virtually no work has been
done on the other biocompounds in algae biolms to date.
3.3.1. Lipids and lipid concentration enhancement
Over the past several decades' neutral lipids have been the main
algae biochemical of interest because of their high concentrations
within the biomass, and because of their conversion to biodiesel
through transesterication. In planktonic systems, algae biomass
can be composed of as much as 70% (g/g dry weight) total
extractable lipids [10]. Total extractable lipids represent a large
family of lipid compounds including polar lipids, neutral lipids, wax
esters, sterols, hydrocarbons, carotenoids, terpenes, quinones, tocopherols, and the various types of chlorophyll compounds [103].
Although many of these lipids have great value, neutral lipids,
mainly in the form of triacylglycerol (TAG), historically were the
lipids of interest. This was because they were the ones primarily
converted into biodiesel [2]. Because of this, many researchers have
targeted these TAGs as the lipid species of interest for biodiesel
production; however, new conversion methods such as hydrothermal liquefaction are increasing promise of converting all extractable
lipids, and some other non-lipid biomolecules, into biocrude [104].
In addition to being a source of fuel, TAGs are valuable to industries
such as the nutraceutical and aquaculture industries.
Triacylglycerol concentrations are species dependent, and under
favorable growth conditions, they represent a fraction of algae
biomass; however, most algae species grown planktonically are
known to signicantly accumulate TAGs in dense lipid bodies in
the cell cytoplasm in response to environmental stress. Although
salinity, pH, temperature, and high CO2 concentrations and light
intensities are stress factors known to affect TAG concentrations in
planktonic algae cultures, by far the most researched, and considered
425
most effective stress factor, is nitrogen and, for diatom species, silicon
nutrient starvation. In their review paper, Hu et al. [103] reported
that planktonic green algae species, on average, increased their total
extractable lipid content from 25.5 to 45.7% (g/g), and diatoms
increased theirs from 22.7 to 44.6%, under stress conditions. Other
researchers have demonstrated similar total lipid accumulation when
exposed to environmental stress [73,105110]. In addition, some
researchers growing algae planktonically have demonstrated lipid
enhancement through photo-oxidative stress [73,107], and increasing carbon dioxide concentrations in growth medium [7,110,111]. In
these studies the lipid accumulation was primarily of TAGs.
The work on lipid accumulation through environmental stress
in algal biolms is much more limited and inconclusive. Schnurr
et al. [24] exposed Scenedesmus obliquus and Nitzchia palea
biolms to bulk mediums decient of nitrogen and silicon, but
could not enhance the neutral lipid concentrations. They attributed this to biolms' inherent ability to accumulate and store
nutrients in the biolm microenvironment, thus not truly starving
the cells of the key nutrients. Similarly, Bernstein et al. [72] and
Kessano et al. [29] reported a lack of signicant neutral lipid
accumulation when they starved algae biolms of nitrate in a
rotating algal biolm reactor. On the other hand, researchers
growing algae biolms on porous membrane materials were able
to signicantly enhance total and TAG lipid concentrations after
cells were starved of nitrogen [2528].
The differences in response to nutrient starvation are likely a
result of how well the biolms were actually starved. First, the ability
to actually starve the biolms could be a function of the mass
transport across the biolm once starvation was commenced, and
that is a function of biolm maturity and composition. For instance,
the researchers [24,29,72] who could not enhance the biomass lipid
concentrations through starvation grew relatively thick algal biolms
(up to 1 mm) on unsterile wastewater medium for extended periods
of time. This wastewater rich in bacteria, microbes, EPS, and inert
solids may, through time, have facilitated the development of
environmentally resilient biolm matrices, which retain nutrients
during nutrient stress periods [41]. Within these matrices key
nutrients are retained via ion exchange resin mechanisms between
nutrients and EPS [40,46]. The researchers [2528] who were
successful in enhancing lipids, on the other hand, grew their biolms
for relatively short periods of time on synthetic medium made from
freshwater sources with minimal concentrations of bacteria and EPS.
This short growth period and freshwater media may have prevented
a well-developed and resilient biolm matrix from forming. The
second factor affecting starvation between the two groups of
researchers may be growth material porosity. In this case the
successfully starved biolms were grown on porous lter paper
membrane materials, thus causing media ow across the biolm
from the material side as well as the water side. This would cause
signicantly more mass transport of nutrients out of the biolm once
the starvation period commenced. The group of researchers who did
not successfully starve their biolms, on the other hand, used rigid
and non-porous growth materials, thus this mass transport was
limited to only a single side of the biolm. For long-term operation of
algae biolm systems, it is unlikely that biolm communities remain
axenic and without well developed EPS matrices, so signicant lipid
accumulation may prove challenging. Future work should further
investigate the nutrient starvation and lipid accumulation mechanisms, but may also consider the potential to accumulate lipids
through other environmental stress factors i.e. increased light intensities, increased CO2 concentrations, etc.
Researchers studying algae biolms for biofuel production have
produced signicantly lower lipid concentrations within their
biomass than researchers growing algae planktonically. One major
reason for this is the method of lipid concentration determination,
and the types of lipids reported. For instance, many algae biolm
426
Table 2
Comparison of lipid concentrations and productivities of species commonly found in freshwater photosynthetic biolms. All values are of organisms grown planktonically
under nutrient replete conditions.
Organism
Species
Biomass Productivities
(g/L/d)
Lipid concentrations
(% w/w)
Lipid Productivities
(g/L/d)
Reference
Bacteria
Cyanobacteria
Cyanobacteria
Cyanobacteria
Cyanobacteria
Diatoms
Diatoms
Diatoms
Green Algae
Green Algae
Green Algae
Green Algae
Escherichia coli
Synechocystis sp.
Unknown
Various species
Spirulina platensis
Nitzhcia sp.
Chaetoceros gracilis
Amphora
Scenedesmus sp.
Chlorella sp.
Scenedesmus obliquus
Chlorella vulgaris
0.0744
0.03
0.21-0.26
0.17-0.20
-
0.7
7.1
7.9-12.6
6.7-10.4
16.0-47.0
36
19.6-21.1
18.4-19.2
11.0-55.0
5.0-58.0
0.002-0.003
0.015-0.048
0.063-0.345
0.041-0.054
0.033-0.037
0.011-0.040
112
113
114
115
68
2. 106, 116
113
1, 116
107
107
2
2
researchers determine their lipid content via chromatography and

report as Fatty Acid Methyl Esters (FAME) [14,17,18,20,21,24,72],
which only account for the methylatable neutral lipid concentrations, whereas some researchers report total lipids through gravimetric analysis [26,27]. Total lipids analysis results in signicantly
higher lipid concentrations because all the extractable compounds
are reported. Another major reason is the composition of algae
biolm biomass compared to planktonic biomass. Mixed community algae biolms generally have much more EPS, bacteria, and
cyanobacteria composing their overall biomass, and these organisms generally have signicantly lower lipid content than algae,
thus bringing the overall biomass lipid content down (Table 2).
Papers reporting lipids data of the same algae species, grown both
planktonically and in biolms, demonstrate this phenomenon
[24,34,72]. Moreover, Shen et al. [28] concluded that the signicantly lower biomass lipid content they produced when growing
with wastewater compared to synthetic media was a result of other
low lipid microorganisms populating the biolms. Table 2 summarizes some of the main types of microorganisms in photosynthetic biolms and their respective lipid contents and overall lipid
productivity potential in planktonic growth systems. It is plausible
that these organisms' growth rates and lipid contents will be
comparable, relative to each other, when they grow in biolms as
well. In order to maximize lipid content and overall lipid productivities of photosynthetic biolms, strategies to maximize proportions
of algae biomass, and even high proportions of high lipid and fast
growing algae species biomass, should be employed.
3.3.2. Algae biolm productivities

Lipid productivities are often calculated by multiplying biomass
productivities (g/m2/d) by the mass fraction of lipids in the biomass;
however, due to various reporting methods, there is a large amount
of variation in overall productivities. Algae biolm biomass productivities are most often reported as dry weight per area of growth
substratum per unit of time, but some report it in terms of dry
weight per area of land used to grow the biomass per unit of time
(areal productivity). The latter reporting method generates signicantly higher productivities because growth substrata can be scaled
vertically in novel biolm photobioreactor growth systems
[14,18,26,27]. Due to the two reporting methods, there is a large
range of values for biomass productivities. Additionally, as mentioned above, some researchers report total lipids rather than FAME
neutral lipids. The variation in reported lipids, coupled with that of
areal vs. substratum productivities, generates substantial variation
of lipid productivities in growth systems (Table 3). Lastly, as shown
in Table 3, researchers often use various reactor designs (with
different nutrient transport and loading rates/concentrations) and

algal species, which signicantly affect overall productivities.
In algae growth systems, increasing lipid productivities through
nutrient starvation is complicated and unpredictable. One major
reason is because there is often a tradeoff between biomass
accumulation and lipid accumulation under these stress conditions. In planktonic algae studies, some researchers have shown
delicate balances of nutrient starvation durations and increases in
lipid productivities [107,110]. In these studies varying starvation
periods would yield either a negative or positive lipid accumulation response, and that response was very time specic i.e. the
timing was delicate. In algae biolm systems Ji et al. [25] found
that maximum lipid productivity was at medium nitrogen concentrations because under those conditions a lipid accumulation
response occurred, and biomass productivities remained high.
Cheng et al. [27] was also able to increase algae biolm lipid
productivities under nutrient decient conditions. In these two
biolm examples, a lipid accumulation response was successful,
causing signicant lipid productivity increases. As suggested earlier in this paper, this was likely possible because the researchers
starved young, axenic, underdeveloped biolms, which were
grown on porous growth substrata. Rodol et al. [107] concluded
that sharp nutrient starvation is necessary to trigger the nutrient
accumulation response in algal cells. Sharp nutrient starvation of
algal cells in a well-developed thick algal biolm may be challenging because of the EPS matrix and its ability to retain nutrients. At
large scale operation it may be extremely challenging to predict
the appropriate time to harvest a starved algae biolm culture.
Lipid productivities of algae biolms have the potential to be
signicantly greater than the best terrestrial crops, especially
when considering vertical scalability. In their review paper, Mata
et al. [2] report biofuel productivities of canola/rapeseed oils to be
approximately 0.25 g/m2/d (calculated from the cited value of
946 kg biodiesel/ha yr). Comparing this value to the lipid productivities in Table 3 shows that algae biolm lipid productivities can
be up an order of magnitude better than conventional terrestrial
biofuel sources if they were grown at on land; however, when
the biolm growth substrata are scaled vertically in novel photobioreactor systems, the lipid productivities are 10100 times more
productive than these crops.
4. Conclusions
Algae biolms have great potential to rapidly grow biofuels and
biochemicals because of their high growth rates and internal
biochemical compositions. Growing the biomass as a biolm, in
427
Table 3
Comparison of biomass and lipid productivities from algal biolm growth systems.
Reporting method
Species
Reactor type
Neutral lipid
concentration (%)
Total lipid
concentrations
(%)
Biomass
productivities
(g/m2/d)
Lipid productivities
(g/m2/d)
Reference
Growth substratum
productivity
Chlorella sp.
Botryococcus
braunii
Nitzchia palea
Scenedesmus
obliquus
Mixed consortia
Scenedesmus
obliquus
Botryococcus
braunii
Mixed consortia
Horizontal at plate
Horizontal at plate
10
9.8
26.8
2.6
0.71
0.26
0.070.2a
[20]
[21]
Horizontal at plate
Horizontal at plate
15
8
2.8
2.1
0.45
0.18
[24]
[24]
Vertical plate airlift

Vertical plate
8
20
2
9.1
0.13
1.82a
[17]
[26]
Vertical plate
43
5.5
2.3a
[27]
12.4
5.5
0.68
[14]
7.7
3.5
0.27
Rotating algal biolm

reactor
Chlorella vulgaris Rotating algal biolm
reactor
Aucutodesmus
Horizontal at plate
obliquus
Botryococcus
Horizontal at plate
braunii
Botryococcus sp. Rotating algal biolm
reactor
Chlorella vulgaris Revolving algal
biolm reactor
Areal productivity
S. obliquus
Vertical plate
B. braunii
Vertical plate
Mixed consortia Rotating algal biolm
reactor
Chlorella vulgaris Revolving algal
biolm reactor
Chlorella vulgaris Rotating algal biolm
reactor
[18]
a
25
39
2.33.6
16.5
4.1
0.68
[28]
7.1
1.8
0.13
[29]
10.2
5.8
0.59
[34]
12.4
20
43
71
49
20
14.2a
21.1a
2.5
[26]
[27]
[14]
10.2
21.5
2.2
[34]
7.7
12.8
0.99
[18]
[25]
Denotes lipid productivities reported as total lipids.
contrast to planktonically, offers potentially signicant advantages

to harvesting, de-watering, and downstream processing the biomass. Drawing from the literature on algae biolm systems
studied in nature and for wastewater treatment, and on the
literature on biofuels production from algae biolm and planktonic systems, there are many things we know to date:
1) Algae biolms can be composed of large quantities of EPS,
bacteria, and other low value biomass depending on biolm
maturity and the growth conditions to which they are exposed.
2) Key growth parameters i.e. light, CO2 concentration, temperature, macronutrients, ow regimes/shear stress, etc., signicantly affects succession and composition of algae biolms.
3) Material properties i.e. hydrophobicity, micro-patterning, etc.,
affect algae biolm growth during early stage development, but
once cell conuence is reached material properties do not
appear to affect long-term growth.
4) Getting optimal amount of light into algae biolms to provide
optimal growth rates is a major challenge for researchers; light
intensity signicantly affects algae biolm growth.
5) Lipid accumulation through environmental stress factors
appears to be more challenging for algae biolms compared
to planktonic growth systems.
6) Species proportions in algae biolms have the potential to
signicantly affect the overall biolm biomass lipid concentrations and productivities.
7) Algae biolm lipid productivities reported as areal productivities (from reactors scaled vertically) are 1-2 orders of magnitude greater than the best terrestrial biofuel crops.
Moving forward it is clear that there are many knowledge gaps
that need to be lled in order to better understand the potential for
algae biolms for biofuel and biochemical production. Particularly, we

want to be able to optimize algae biolm biomass productivities, and
biochemical concentrations within these biolms. Even in its research
infancy, the production of biofuels and biochemical from algae biolm
growth systems shows great potential; targeting the knowledge gaps
outlined in this paper will help explore this potential.
Acknowledgments
The authors would like to thank the Natural Science and
Engineering Research Council of Canada (NSERC) for nancial
support in the form of a Strategic Grant (#STPGP 380795-2009),
and a Canadian Graduate Scholarship (CGSD). Additional thanks to
HATCH Ltd. for nancial support in the form of a Graduate Student
Scholarship for Sustainable Energy Research.
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Factors affecting algae biofilm growth and lipid

125 PUBLICATIONS 2,156 CITATIONS

All in-text references underlined in blue are linked to publications on ResearchGate,

Available from: Peter Schnurr

Renewable and Sustainable Energy Reviews 52 (2015) 418429

Contents lists available at ScienceDirect

Renewable and Sustainable Energy Reviews

Factors affecting algae biolm growth and lipid production: A review

Corresponding author. Tel.: 1 416 978 8517.

Algae growth systems show great potential for the production

high concentrations of valuable biocompounds. Coupled together,

review such as this is important as algae biolm biofuel and

2. Composition and structure of an algal biolm

2.1. Extracellular polymeric substances and matrices

2.2. Species and succession of photosynthetic biolms

medium, and how they respond to the particular abiotic growth

cyanobacteria is known to thrive under higher temperatures

3. Algae biolm biomass and lipid production

recruitment to the growth material; however, the groups reporting

3.1.2. Biotic factors on biolm development and growth

biolm [56,61], so depending on its thickness, a large proportion of

Vertical at plate PBR

3.2.2. Carbon dioxide concentrations

3.2.3. Other growth factors

accumulation and overall growth rates [31,35,63], but these growth

researchers determine their lipid content via chromatography and

3.3.2. Algae biolm productivities

different nutrient transport and loading rates/concentrations) and

Vertical plate airlift

Rotating algal biolm

Denotes lipid productivities reported as total lipids.

contrast to planktonically, offers potentially signicant advantages

algae biolms for biofuel and biochemical production. Particularly, we

carbon and nutrient removal from domestic wastewater. Ecol Eng

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