Chloroplast Evolution in Red and Blue Algae

7/31/2019 Chloroplast Evolution in Red and Blue Algae

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Chloroplast evolution, divergence, and functional maintenance in algae and plants:

adaptations and implications for carbon sequestration, improved crop productivity and

global warming

Abstract:

Chloroplasts are the organelles within photosynthetic organisms that are

responsible for photosynthesis. They are descended from cyanobacteria, and wereincorporated into eukaryotes via endosymbiosis. Green algae are the most ancestral of the

photosynthetic eukaryotes and gave rise to both red algae and land plants, two very

different groups. The primary endosymbiotic event likely took place between an ancestor

of current green algae and a cynaobacterium. Since then the chloroplasts in the red algal,green algal, and land plant lineages have diverged significantly from each other, especially

in regards to their proteins and pigments.

Rubisco stands out as the most important chloroplast protein. It catalyzes the

fixation of carbon, and is a particularly challenged enzyme: it is likely to perform thefixation of oxygen, which is a detrimental reaction, when oxygen competes with carbon

dioxide for the enzymes active site. The mechanisms algae and plants have developed todeal with this enzymatic problem are indicative of their particular environmental

challenges. In regards to their pigments, each of these lineages has evolved to best utilize

the light wavelengths available to them. Land plants can capture enough light with mostlychlorophylls, so they do not need to maintain a wide range of accessory pigments. Marine

algae live a light-limited environment, so they must utilize a range of accessory pigments

to capture sufficient light. Trans-membrane transport systems and strategies for preventing

photoinhibition and photorespiration also differ among these lineages.Algae and plants live in distinct environmental niches, and understanding the

adaptations of their photosynthetic systems to these environments can help us understandhow these various primary producers may respond to challenges such as global warming.

Keywords:

Chloroplasts, photoinhibition, photorespiration, Rubisco, red algae, green algae, land

plants, Tic/Toc translocation, pigments, light harvesting complexes


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Introduction

Chloroplasts are the central organelles for the production of energy across Plantae.Today's chloroplasts began as independent organisms that were captured by an early

ancestor of plants and algae at least 1.6 billion years ago. 1,2,3,4Numerous efforts have been

made to document the evolution of chloroplasts across the plant and bacterial kingdoms,and it is believed that chloroplasts are likely descended from primitive forms of

cyanobacteria which were incorporated into eukaryotes through a single endosymbiotic

event.5,6 Chloroplasts operate using a variety of processes with the primary functions of theorganelle being the production of energy and the fixation of carbon. In order to

successfully manufacture organic compounds in the many environments inhabited by

plants and algae, chloroplasts necessarily have evolved to suit the circumstances of these

diverse groups. 7,8,9,10

There are many reasons to be interested in chloroplast processes, among which are

their role as the primary energy producer for life on earth, curiosity about the origins and

relations of cellular organisms, and even hopes of using genetic engineering to improve

chloroplast metabolic processes to raise crop yields and address global warming throughoptimization of CO2 extraction from the atmosphere.11 Plants and algae have spent

approximately one and a half billion years adjusting to atmospheric changes, specializing,and evolving to function across the many environmental niches of the planet. Among the

key photosynthetic processes that have been tuned and adjusted in the evolutionary process

is the Calvin cycle. Within that cycle, a particular family of proteins known as Rubisco isboth essential and seemingly flawed in their function. Rubisco is essential in carbon

fixation, but it operates only under very

constrained conditions, conditions limited by

the availability of CO2 or bicarbonate andunder the constant threat of mis-function, as

Rubisco is nearly as attracted to O2 as it is to

CO2.12

Green algae are the ancestors of all

plants and other algal groups, including the

red algae (Figure 1).1 Green algae are moreclosely related to land plants than to red

algae, though both types of algae are marine.

This indicates that red and green algae have

developed distinct mechanisms for survivingin similar habitats. Land plants survive in a

particularly different environment from either

algae group. These three groups differ insome of their basic chloroplast proteins: the

light-harvesting complexes and those proteins

used to prevent photorespiration andphotoinhibition. 13

Chloroplast Evolution:

Figure 1: This shows the evolutionary history of red

algae, green algae (the Chlorophytes and

Charophytes), and land plants (the Bryophytes,

Ferns, Gymnosperms, and Angiosperms).1 There

was only one endosymbiotic event for all Plantae,

and it occurred with the incorporation of a

cyanobacteria (CB) by an early eukaryote. The

secondary endosymbiotic event led to the

divergence of brown algae, among otherphotosynthetic species.


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All of the photosynthesis within plants and algae is performed by chloroplasts,

which are semi-independent organelles derived from photosynthetic bacteria.14 These

bacteria were incorporated into an ancestor of plants and algae via phagocytosis. Thisengulfment and incorporation of the photosynthetic bacteria by an ancestor of

photosynthetic eukaryotes is known as endosymbiosis and is believed to have occurred

around 1.6 billion years ago.1 There was only one primary endosymbiotic event thatresulted in the chloroplasts for Plantae.5 Over time, the chloroplasts within the various

algal and plant lineages have diverged from each other, but they continue to serve the same

fundamental role within their hosts.Land plants and other algal lineages are descended from green algae.1 Plantae,

which is the kingdom that encompasses green and red algae and plants, is monophyletic

(Figure 1).5,15 All of the chloroplasts throughout Plantae have a common cyanobacteria

ancestor resulting from a single primary endosymbiotic event. Despite the fact that thechloroplasts all derive from a single ancestor, there is a great deal of variation among the

chloroplasts of green algae, red algae, and land plants. An example of this is the number of

grana per stack in a thylakoid: red algae have single grana, while both green algae and

plants have multiple granaper stack.16 This variation is

also evident in thedifferences in translocation

mechanisms between

chloroplasts and their hostsand in the diversity of the

Rubisco proteins found

within Plantae.

Chloroplasts nowcontain only a small

number, from 50 to 200, of

their original component ofgenes.17 The other one to

two thousand proteins used

in chloroplasts are nowencoded for by genes in the

nuclei of the host

eukaryotes. The fact that the

hosts manufacturechloroplast proteins

indicates that there must be

mechanisms to transferthese proteins into the

chloroplasts. One example

of such a mechanism is theToc and Tic

translocators (the translocon

at the outer chloroplast

envelope and the transloconFigure 2: Diagram of the evolution and current state of the

Toc/Tic translocator systems found in Plantae lineages.6C.

reinhardtiiis the green alga.


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at the inner chloroplast envelope, respectively). Many of the proteins involved in these and

other complexes are homologous among green algae, red algae, and plants, but there are

significant differences in the number and type of proteins involved.The Tic/Toc translocator system, for example, is mostly conserved across groups,

but there have been important changes in the alternate evolutionary paths.18Toc proteins

have been particularly conserved between the green algae and plants. There are fifteenmajor proteins involved in the vascular plant Toc system. Of these, two are present solely

in the plant lineages, and one of the proteins is slightly modified from the green algal

version.19,20,21 Thus, the mechanism for translocation across membranes functions mostlythe same for these two groups. Red algae are more modified compared to land plants than

the green algae, but the system is still quite similar (Fig. 1).

Another example of variation in photosynthetic eukaryotes proteins is Rubisco.

The types of Rubisco among these groups appear to be descended from three major plastidlineages. Green algae and plants contain Rubisco-encoding genes from a single lineage that

is related to cyanobacteria, and red algal Rubisco-encoding genes come from a distinct

other lineage that is

more closely related toproteobacteria.22 These

distinctions areparticularly based on

differences among the

rbcL genes (whichencode the large

subunit of Rubisco and

are located within the

chloroplast) and arenot observed in other

proteins. The fact that

the Rubisco-encodinggenes are divided into

multiple evolutionary

lineages (i.e. that theyare polyphyletic) is in

contrast with other

chloroplast lineage

determinations, whichdemonstrate that these

plastids have a

monophyleticbackground.5 Thus,

there is some support

for the idea that therewere either multiple

horizontal gene transfer events between photosynthetic groups or gene duplications leading

to paralogous Rubisco-encoding genes in these groups.23

Figure 3: The larger yellow circles represent endosymbiotic events,

either primary or secondary.25 The smaller yellow circles represent

gains of LHC genes. The red squares represent the loss of LHC genes.

In particular, note that all groups except the red algae and theGlaucophytes (freshwater algae) lost PBP, phycobilin proteins. Green

algae are the Chlorophyceae and Ulvophyceae. Land plants are the

Embryophytes.


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The type of Rubisco contained by each of these groups has been classified in detail.

All of the photosynthetic eukaryotes have chloroplasts that contain form 1 of Rubisco,

which is distinct from the Rubiscos found in dinoflagellates and Archaea (Lisa M Nigro,Masters thesis, The Graduate School, University of Maine, 2006). There are four subgroups

of Rubisco within form 1: 1A, 1B, 1C, and 1D. Plants and green algae contain form 1B.

Red algae mostly contain form 1D but have also been found to contain form 1C. There islittle variation in the sequences of form 1B, and form 1C contained much more genetic

variation. These distinct Rubiscos have differing affinities for CO2 and varied rates of

fixation.24 Though Rubisco has been modified across Plantae, the Calvin Cycle, the majorpathway for carbon assimilation, is mostly conserved in all photosynthetic organisms.11

Light Harvesting Complexes (LHCs) and Pigments:

LHCs demonstrate both evolutionary connections between the algae and plants andadaptations to environmental conditions. These complexes are composed of pigment-

binding proteins.25 Though there are comparable LHC structures in green algae and plants,

the antennae systems in these two groups likely evolved independently since there are few

shared orthologs. Green algae have a lager photosystem I (PSI) complex, with ninepolypeptides, whereas plants PSI uses six polypeptides (Table 1).

There are two types of pigments in green algae and plants, chlorophyll andcarotenoids, and an additional family of pigments in red algae called phycobilins. Plants

and algae use carotenoids in photoprotective roles and dissipate excess excitation energy

through them in a process known as non-photochemical quenching (NPQ).26 There are over600 known carotenoids. Those used in the xanthrophyll cycle differentiate plants from

algae.27 Red light, which is absorbed by both chlorophylls a and b, is limited in its

penetration of water. Green algae compensate by absorbing more green light through their

carotenoids.28 Phycobilins, which absorb light in the green and yellow wavelengths, arethe primary light harvesting pigments of red algae, which typically live in a more light-

limited environment than green algae or plants (Figure 4).

Figure 4: These show (a) the depth to which particular wavelengths of light penetrate the ocean and (b)

the absorbance spectra of various pigments found in algae and plants. Also in (b) the black line represents

the (a) is from

http://oceanexplorer.noaa.gov/explorations/04deepscope/background/deeplight/media/diagram3.htm, and

b. is from http://course1.winona.edu/sberg/ILLUST/fig15-5.jpg.


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The core antennae system of the light harvesting compounds developed early in

green algae evolution and included chloroplast proteins that today are functionally involved

in PSI and PSII across all green algae and plant species. The core antennae system includeschloroplast proteins 29 and 26 (CP29 and CP26), which are coded for by light harvesting

complex genes Lhcb4 and Lhcb5, respectively (Table 1). CP26 and CP29 are associated

with PSII and are present in green algae and higher plants. There exist, however,chloroplast proteins specific to green algae with early evolutionary roots, as demonstrated

in their widespread presence in algal species, which are not present in higher plants. Light

harvesting complex genesLhca2 andLhca9 are green algae specific, and the fact that thereis no evidence of them in red algae demonstrates that red and green algae diverged early.

Chlamydomonas reinhardtii, the model green alga, contains 11 light harvesting complex

genes that program for LHCI, whileArabidopsis thaliana, the model plant, only contains 3

genes that perform corresponding work.29

Photorespiration:

Photorespiration in plants and algae is impacted by the types of Rubisco and the

carbon concentrating mechanisms (CCMs) that the respective groups have evolved.There are four major classes of Rubisco. The Rubisco found in plants and nearly all algae,

form1, discriminates poorly between oxygen and carbon dioxide.22 Algae and plants usedifferent CCMs. In land plants, there are two main methods for dealing with Rubiscos

low specificity: C3, and C4 photosynthesis. Plants with C3 use a form of Rubisco that is

more specific for carbon dioxide.24 C4 plants have developed cellular processes that resultin higher concentrations of carbon dioxide around Rubisco, so the enzymes specificity

does not matter as much. Algae have increased requirements for carbon concentration over

plants since water contains a lower concentration of CO2 than air30,31 Many algae have

developed carbon concentrating mechanisms to help deal with the issue ofphotoinhibition.24,32,33,34 Those algae that have not developed such mechanisms have forms

of Rubisco with a higher affinity for CO2. The type of Rubisco found in red algae also has a

lowered affinity for O2. . Both plants and algae use CCMs to increase the concentration ofCO2 around Rubisco so that the enzyme will preferentially bind CO 2 instead of O2. Marine

algae do not appear to be carbon-limited with their CCMs maintaining steady cellular

access to carbon in variable environmental conditions. 35Within algae, there are multiple levels of carbon concentration. There is evidence

for active transportation of inorganic carbon, either in CO2 or HCO3- (bicarbonate) form,

across the chloroplast membranes and across the pyrenoid membranes in algae. The

diffusion of carbon dioxide in water is 104 times slower than in air, consequently algaemust actively transport CO2 into their cells, in contrast with the passive diffusion of CO 2into C3 plants.

36 One of the main problems for marine algae is that the carbon available in

water exists mostly as HCO3-.37 Thus, it must be converted to CO2 before being used by

Rubisco. Marine algae use carbonic anhydrase to perform this reaction. Rubisco may also

exist freely in the stroma or be localized within a pyrenoid.

The efficiency of Rubisco is not only dependent on CO2 concentrations but also onthe surrounding temperature. Heat stress can result in the decrease in efficiency of

Rubisco.38 This occurs through the deactivation of Rubisco activase and the subsequent

decrease in activity of Rubisco. Increases in temperature can also lower the exchange rate

of CO2 across membranes, which further negatively impacts Rubisco.39, 40


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Photoinhibition:

Photoinhibition is a significant problem for plants and to a lesser extent also affectsmarine algae. When plants and algae are exposed to extreme conditions, from heat stress to

drought to excess light, they can suffer from photoinhibition.41 This means that the electron

transport chain (ETC) of photosynthesis, involved in the production of a proton motiveforce (pmf), is functioning non-optimally. The ETC is being damaged faster than it can be

repaired. The damage is believed to result from the evolution of radical oxygen species,

which slow the rate of protein production and thus slow the rate of repair to systemsdamaged by stress from excess energy uptake. Two of the main mechanisms for

photosynthetic organisms to defend themselves from excess light energy are regulating the

rate of photosynthesis and dissipating heat through NPQ.

State transitions are regulatory mechanisms that are used to balance the activities ofPSII and PSI in order to optimize photosynthesis under variable conditions.42 State

transitions are used to prevent reactive oxygen species from forming. State transitions refer

to the phosphorylation and movement of the light harvesting complexes (LHC) from PSII

to PSI and back. This transfer of the LHCs is a mechanism for equilibrating the output ofthe two photosystems. This process is moderated by the relative rates of reaction of the

photosystems and so is dependent on the amount of light available. When LHCs arephosphorylated, some of them move from PSII to PSI. In plants, only about fifteen percent

of the LHCs migrate to and from the PSI. In algae, up to eighty percent of the LHCs can be

transferred. This system works both to maximize photosynthetic output and protect theorganism from the effects of photoinhibition. The process is catalyzed by a protein kinase;

in plants it is called STN7 and in algae Stt7.43,44,45,46There is a high degree of similarity

between these proteins, but their efficiencies and results are markedly different.47

Another method of alleviating photoinhibition via regulation of the photosyntheticrate is cyclic electron flow.48 This cycling of electrons around PSI takes place when the

damage to PSII is occurring faster than the rate of repair. PSII, and especially its D1

protein, is the preferential site of damage during photoinhibition. Damage to the D1 proteinshuts down the electron transport chain and thus prevents the formation of reactive oxygen

species. This pattern is conserved across algae and plants. When cyclic electron flow is

inhibited, the rate of damage to PSII goes up under high light conditions. The formation ofa pmf continues under cyclic electron flow, but there is reduced conversion of NADP+ into

NADPH or of ADP into ATP. This is the problem with photoinhibition prevention

systems: they protect the photosystem proteins from damage but at the cost of a lower

photosynthetic yield.A third method of preventing photoinhibition is heat dissipation (i.e. NPQ). CP24 is

the most recently evolved minor antenna complex in PSII, and is found solely in land

plants.49 It is believed to play a role in NPQ, particularly in the conversion of violaxathin tozeaxanthin. This reaction is central to the dissipation of heat, retarding photoinhibition.50

Green and red algae have alternate methods of NPQ since they do not have CP24 as plants

do.49 Algae are not exposed to as much heat stress as plants (this is due to the differentheat capacities of the ocean versus the atmosphere), so they do not need the most efficient

protection against photoinhibition. They instead contain CP26, which is an ancestral

protein to CP24. CP26 is also found in plants, and performs the same basic function as


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CP24: the production of zeaxanthin to defend the organism from excess light energy.

CP26, however, is not as efficient at catalyzing this reaction.25,51.

Photoinhibition is a common issue for both plants and algae. For algae, lightintensity can vary dramatically during normal wave action and over tidal cycles and result

in light stress.52 Similarly for plants, light and heat levels can increase over the course of

the day and stress the photosynthetic systems.53

Because plants are primarily land-basedand green and red algae are marine organisms they necessarily have to deal with different

levels of stresses. The differences in environmental conditions permit algae to utilize less

efficient systems than plants to mitigate the effects of photoinhibition.

Conclusion:

Red algae, green algae, and land plants, though they belong to a monophyletic

group and have chloroplasts which perform similar functions, are distinct groups. Therewas only one endosymbiotic event which resulted in the formation of chloroplasts for all

photosynthetic eukaryotes. However, the chloroplasts for each group have diverged from

the others to better suit the environments of their hosts. All of these strategies for

photosynthesis may be affected by global climate change in the future,Global warming is predicted to have dramatic effects on photosynthesis,

particularly in regards to photoinhibition.54 The movement of CO2 into a plant, or throughwater, is dependent both on the concentration of CO2 in the surroundings and the

temperature. At temperatures higher than the current climate, even with an increase in CO2concentration, Rubisco has been shown to be less efficient. Since both temperature andCO2 levels will change in the coming years, the impact on photosynthetic organisms may

be significant. Due to the importance of photosynthesis to the biosphere, understanding the

various mechanisms that photosynthetic organisms have evolved to perform this function is

imperative.


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Table 1: A synthesis of the differences between green algae, red algae, and land plants in

regards to photosynthetic and chloroplast machinery.Green Algae Land Plants (vascular) Red AlgaePigments16 Chl a

Chl b

carotenoids (examples):

xanthophyll

violaxanthin

neoxanthin

lutein

loroxanthin-

Chl a

Chl b

carotenoids

xanthophyll

violaxanthin

-

Chl a

-

carotenoids

xanthophyll

violaxanthin

phycobilins:

phycocyanin

phycoerythrin

LHC Proteins

(genes)25,55,56,57

minor antennae

proteins

LHCII type 1 (Lhcbm1-6)

LHCII type 2 (Lhcbm8-9)

LHCII type 3 (Lhcbm11)

LHCI type 1 (Lhca1)

-

LHCI type 3 (Lhca3)

LHCI type 4 (Lhca2)

LHCI type 5 (Lhca4-8)LHCI type 6 (Lhca9)

LHCQ (Lhcq andLI818)

-

CP29 (Lhcb4)

CP26 (Lhcb5)

-

LHCII type 1 (Lhcb1)



LHCI type 1 (Lhca1)

LHCI type 2 (Lhca2)

LHCI type 3 (Lhca3)

LHCI type 4 (Lhca4)

LHCI type 5 (Lhca5)LHCI type 6 (Lhca6)

LHCQ (Lhcq)

-

CP29 (Lhcb4)

CP26 (Lhcb5)

CP24 (Lhcb6)

LHC1 (Lhcar1)*

LHC1 (Lhcar2)

LHC1 (Lhcar3)

LHC1 (Lhcar4)

LHC1 (Lhcar5)

(Lhcf4)

Kinase for the state

transition of LHC58Stt7 STN7 Stt7

Toc/Tic translocator

proteins1680

159

75

34

-

-22

-

21

20

11040

55

32-

62*

ClpC

80/75 (alt. combination)

159

-

34

-

-22

22*

21

20

110-

-

32-

62*

ClpC

80

159

75

34

64

1222

-

21

20

11040

55

3262

-

ClpC

* These genes and proteins correspond directly with those in green algae and plants. Red algae have notbeen extensively studied in this regard: analysis of their protein sequences and LHCs is still underway.59


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They do have CP26 and CP29, but not CP24, similar to green algae, but the genes encoding these minor

antennae proteins do not appear to be known in red algae.


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Chloroplast Evolution in Red and Blue Algae

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