Turning the aquatic weed Azolla into a sustainable crop

219 Pages·2017·20.72 MB·English

Turning the aquatic weed Azolla
into a sustainable crop
Layout by Kimberley Piek
Cover photo | design: Ronald Leito | Kimberley Piek
Printed by ProefschriftMaken || www.proefschriftmaken.nl
ISBN: 978-90-393-6788-9
LPP contribution series: 48
The reserach described in this thesis was funded by the University of Utrecht and
the Laboratory of Paleobotany & Palynology (LPP) Foundation. Additional financial
support was provided by Climate KIC.
Turning the aquatic weed Azolla into a sustainable crop
De transformatie van het aquatische onkruid Azolla
tot een duurzaam gewas
(met een samenvatting in het Nederlands)
Proefschrift
ter verkrijging van de graad van doctor aan de Universiteit Utrecht op gezag van
de rector magnificus, prof. dr. G.J. van der Zwaan, ingevolge het besluit van het
college voor promoties in het openbaar te verdedigen op vrijdag 7 juli 2017
des avonds te 6.00 uur
door
Paul Brouwer
geboren op 28 april 1988 te Utrecht
Promotoren: Prof. dr. J.C.M. Smeekens
Prof. dr. G-J. Reichart
Copromotoren: Dr. H. Schluepmann
Dr. K.G.J. Nierop
Table of contents
Chapter 1 9
General introduction
Chapter 2 31
Azolla domestication towards a biobased economy?
Chapter 3 57
Profiles of diel molecular responses to N fixation by Nostoc azollae reveal
2
that metabolic, structural and vascular cooperation sustain the high
productivity of Azolla ferns without nitrogen fertilizer
Chapter 4 81
Maintaining productive cultures of Azolla: methodology and the effect of CO
2
concentrations and species on biomass yield, chemical composition and
suitability as feed
Chapter 5 101
Lipid yield and composition of Azolla filiculoides and the implications for
biodiesel production
Chapter 6 115
Phenolic compounds and their biosynthesis pathways in the aquatic fern
Azolla
Chapter 7 151
Extracting protein from tannin-rich Azolla
General discussion & outlook 173
References 183
Summary 208
Nederlandse samenvatting 211
Dankwoord | Acknowledgement 215
Curriculum Vitae 221
8
Turning the aquatic weed Azolla into a sustainable crop
9
Chapter 1
General introduction
10
Demand driven by a growing and wealthier world
population
Over the last decades the human population on Earth has expanded exponen-
tially from approximately one billion people in 1800 to 7.3 billion in 2015 (United
Nations, 2015) and is expected to reach more than 9 billion by 2050 (United Nations,
2015; Lukovenkov et al., 2011). The rate of population growth is decelerating and
a major driver of this deceleration is increased wealth (Godfray et al., 2010). Pro-
ducing sufficient food for the additional 1.7 billion people in the next 33 years will
become a major challenge, whereas today still 12.9% of the global population is
undernourished (FAO et al., 2015). Higher purchasing power additionally results in a
higher consumption and a greater demand for meat, dairy, and fish (Godfray et al.,
2010; Speedy, 2003). The production of meat and dairy requires a 2.3 up to 13 fold
input of grains as feed and thereby puts even more pressure on global food supply
(Sabaté and Soret, 2014), whereas global fish stocks are declining due to overex-
ploitation (FAO, 2016). Not only does increased wealth results in higher demand for
food and feed, also the consumption of energy (Ferguson et al., 2000) and materials
(Wiedmann et al., 2015) have a positive correlation to wealth. Hence a growing and
wealthier world population will boost future demand for food, energy and materials,
increasing pressure on Earth’s ecosystem.
Negative environmental impacts of current
production systems
The negative environmental impacts of our production systems are becoming in-
creasingly well understood and more tangible. Since the start of the industrial revolu-
tion in 1760, mankind has used vast quantities of fossil fuels to power the production
of food and commodities, as well as to provide for transportation, heat and, more re-
cently, electricity. Before the industrial revolution, CO drawdown by photosynthesis,
2
weathering and ocean sedimentation, and CO emission from respiration, freshwater
2
outgassing and volcanism were in balance (Ciais et al., 2013). The amount of carbon
stored in the atmosphere is only small compared to the carbon locked in soils, fossil
fuel reserves, and especially oceans (Ciais et al., 2013). However, due to a slow net
exchange between the atmosphere and other reservoirs, it may take decades to
thousands of years until atmospheric CO is relocated into terrestrial and ocean car-
2
bon resevoirs (Ciais et al., 2013). The burning of fossil resources within a limited time
frame has therefore led CO piling up in the atmosphere. In 2015 the average CO
2 2
concentration measured at the Mauna Lao observatory station exceeded 400ppm,
versus 317 ppm in 1960 and 200ppm during pre-industrial times (Keeling, 2008).
The emission of CO and other greenhouse gasses (GHGs) by humans has caused
2
Turning the aquatic weed Azolla into a sustainable crop
Chapter 1 11
global temperature to rise 0.8 °C and resulted in more extreme weather events such
as heat waves, droughts, floods, cyclones, and wildfires, melting of glaciers and sea
ice and changing migration patterns for wildlife (IPCC, 2014). Consequently, these
climatic changes have negative socio-economic impacts, such as loss of crop yields,
material damage and decreased availability of drinking water (IPCC, 2014). If emis-
sions of greenhouse gasses are not reduced, global temperature may rise more than
4°C compared to 1900, along with an exponential increase in associated impacts on
environment and societies (IPCC, 2014).
Between 1960 to 2000 global grain production increased from 1 billion to 2 billion
tons per year, a period often referred to as the ‘green revolution’ (Khush, 2001). A
major breakthrough enabling this ‘green revolution’ was the development of crop
varieties with improved response to nitrogen fertilizer (Khush, 2001). Effectively,
the use of artificial fertilizer has increased 7 fold over this period (Tilman, 1998).
Concomitantly, the production of nitrogen fertilizer by the Haber-Bosch process has
increased terrestrial N input by 71% and global N input by 34% (Figure 1) (Gruber
and Galloway, 2008). The nitrogen fertilizer is only partly incorporated in the plant
biomass, as 16% of the nitrogen input into croplands may leach into the freshwa-
ter hydrological cycle and another 20% is emitted to the atmosphere in gaseous
form (Wang et al., 2017). Additionally, a large share of the nitrogen in the harvested
biomass, which serves human consumption, is excreted and ends up in freshwater
bodies (Gierlinger, 2014; Cease et al., 2015).
The increased use of nitrogen fertilizer from 1960 onwards was accompanied
by the use of phosphorous fertilizer. Unlike nitrogen, phosphorous is a much less
mobile element. Volatilization is negligible and it is hardly present in a soluble form
as it quickly precipitates (Smil, 2000). Run-off of phosphorous from land to oceans
proceeds therefore mainly due to erosion and as particulate P (Smil, 2000). Once
in the ocean, phosphorous is buried in marine sediments at rates of 25-35 M ton
year-1 (Smil, 2000). The slow process of tectonic uplift is required to bring this P back
to land surfaces. Effectively, natural ecosystems depend on very efficient recycling
of the available phosphorous. By mining ancient phosphorous sediments, mankind
adds 15 Mt year-1 of phosphorous fertilizer to the global phosphorous cycle, repre-
senting 52-58% of the total phosphate input of croplands (Smil, 2000).
Intensive use of artificial fertilizers has more than doubled nitrogen and phos-
phorous run-off into freshwater, and eventually marine ecosystems (Figure 1) (Gru-
ber and Galloway, 2008; Smil, 2000). The run-off of phosphorous and nitrogen into
fresh-water ecosystems promotes the growth of few species adapted to a high
nutrient environment and inhibits growth of species that are limited by other factors,
thereby decreasing biodiversity (Erisman et al., 2013). The same process occurs in
coastal areas where high nutrient runoff entering the oceans causes algal blooms.
By fueling microbial respiration, algal blooms can furthermore lead to coastal zones
12
xes vid-s of ous
mbers in red indicate fluais et al. (2013) and prod provided in million tonmillion tons of phosphor
cles. Nun from Ci2008) anvided in
hosphorous (P) cyon fluxes are takeuber & Galloway (mil (2000) and pro
nd pcarbm Grm S
arbon (C), nitrogen (N) ae natural fluxes. Data for n fluxes are adapted frous fluxes are adapted fro
al ccatogeoro
activities on globack numbers indiet al., 2013). Nitry, 2008). Phosph
n bls a
ence of humaactivity, whilst n carbon (Ciaier and Gallow
InfluFigure 1. due to human ed as billion tonitrogen (Grub(Smil, 2000).
Turning the aquatic weed Azolla into a sustainable crop