BIOC0004 Lecture 2: Evolution of Eukaryotic Algae and Endosymbiotic Theory

Evolution of the First Photosynthetic Eukaryote

• Historical Context: Molecular analysis of chloroplast genes in both plants and algae indicates that the organelle originated from a cyanobacterium approximately $1$ billion years ago.
• The Mechanism of Phagocytosis: The process by which a cell engulfs particles includes several stages:
  • Pseudopods: Extensions of the cell membrane used to surround the bacterium.
  • Phagosome (Food Vacuole): The vesicle formed around the engulfed bacterium.
  • Phagolysosome: The result of a lysosome fusing with the phagosome to initiate digestion.
  • Digestion and Post-digestion: The breakdown of the organism for nutrients.
• Endosymbiotic Theory (Primary Endosymbiosis): This occurs when phagocytosis "goes wrong," leading to a symbiotic relationship rather than digestion.
  • The Event: A free-living cyanobacterium was engulfed by a feeding, amoeba-like eukaryote.
  • The Relationship: The cyanobacterium became an endosymbiont. It provided fixed carbon through photosynthesis and oxygen to the host. In exchange, the host provided a safe, nutrient-rich niche.
  • Evolutionary Transition: Over time, the relationship shifted from a facultative symbiont to an obligate symbiont, and finally to a permanent organelle (the chloroplast).
• Photosynthetic Equation: The process established by this symbiosis is represented by: $6CO_2 + 6H_2O + \text{sunlight} \rightarrow C_6H_{12}O_6 + 6O_2$
• Biological Synchronization: The survival of the new organism required the replication of the endosymbiont to be synchronized with the replication of the host.

Selective Pressures and Genome Reduction

• Ancestral Genome: The free-living cyanobacterial ancestor possessed several thousand genes.
• Selective Pressures for Gene Loss:
  • Redundancy: Genes no longer required for an endosymbiotic life (e.g., genes for flagella, cell walls, or scavenging micronutrients) were quickly lost.
  • Duplication: Genes for metabolic pathways that were already present in the host (duplicated efforts) were discarded by the symbiont.
  • Endosymbiotic Gene Transfer (EGT): Many genes were transferred from the cyanobacterium to the host cell's nucleus.
• Modern Chloroplast Genome Status:
  • Modern chloroplasts typically contain a circular genome of only $100-200$ genes.
  • The genome size is approximately $\sim 3,600\,\text{kb}$.
  • This represents a roughly $90-95\%$ reduction in size and gene complexity compared to the original cyanobacterial genome.

Primary Endosymbiosis Lineages

• Extant Lineages: Primary endosymbiosis resulted in three distinct lineages of algae:
  • Glaucocystophyta (often referred to as "glaucos").
  • Chlorophyta (Green Algae or "greens").
  • Rhodophyta (Red Algae or "reds").
• Evolution of Pigment Composition:
  • Chlorophyta: Chl. a, Chl. b.
  • Glaucocystophyta: Chl. a, phycobilins.
  • Rhodophyta: Chl. a, phycobilins.
• Significance of the Chlorophyte Lineage:
  • This lineage gave rise to all land plants.
  • Studies (e.g., Herron et al., 2019) examine the de novo origins of multicellularity in response to predation.
  • The progression toward complexity involves: Chlamydomonas (unicellular) $\rightarrow$ Gonium $\rightarrow$ Volvox (multicellularity and cell differentiation).

Glaucocystophytes and the Peptidoglycan Layer

• Characteristics: A relatively insignificant group of freshwater algae with only about $13$ described species.
• Evolutionary Importance: They have retained the peptidoglycan (PG) cell wall of the original Gram-negative cyanobacterial ancestor within their chloroplasts.
• Structural Layers: The chloroplast structure consists of an inner membrane, a peptidoglycan cell wall, and an outer membrane.
• Comparison with Other Lineages:
  • Glaucophytes: Possess genes for PG synthesis.
  • Red and Green Algae: Lack PG genes.
• Antibiotic Sensitivity: Evidence of this vestigial wall is shown by the fact that $\beta$-lactam antibiotics, which disrupt bacterial cell wall synthesis, can affect the synthesis of the glaucophyte chloroplast.

Secondary Endosymbiosis: The "Russian Doll" Model

• Definition: The process of acquiring a "second-hand" chloroplast by one eukaryote engulfing another photosynthetic eukaryote.
• Step-by-Step Process:
  1. Capture of a photosynthetic eukaryote.
  2. Establishment of a symbiont.
  3. Reduction of the symbiont to an organelle via gene transfer and the creation of a nucleomorph.
  4. Eventual loss of the nucleomorph.
• Membrane Structure: This process results in chloroplasts surrounded by $3$ or $4$ membranes ($2$ from the original chloroplast, $1$ from the engulfed eukaryote's plasma membrane, and $1$ from the host's phagosomal membrane).
• The Green Lineage (Secondary):
  • Chlorarachniophyta: Features a nucleomorph and $4$ membranes.
  • Euglenophyta: Results in $3$ membranes; the host for the green alga endosymbiosis was closely related to modern-day trypanosomes.
• The Red Lineage (Secondary):
  • Cryptophyta: Features a nucleomorph.
  • Heterokontophyta: Includes kelps, diatoms, and chrysophytes.
  • Haptophyta: Includes coccolithophorids.
  • Dinophyta (Dinoflagellates).
  • Apicomplexa.

Remarkable Features of Chlorarachniophytes and Cryptophytes

• Commonality: Both groups retained a nucleomorph, a vestigial eukaryotic nucleus.
• Genome Complexity: These cells possess four separate genomes, each with a different evolutionary history:
  1. Nuclear genome: From the eukaryotic host.
  2. Nucleomorph genome: From the eukaryotic alga endosymbiont.
  3. Chloroplast genome: From the cyanobacterium.
  4. Mitochondrial genome: From an $\alpha$-proteobacterium.
• Convergent Evolution: Despite different origins (Chlorarachniophytes from green algae; Cryptophytes from red algae), their nucleomorph genomes show striking similarities:
  • They are miniaturized into three tiny chromosomes.
  • They consist of a few hundred genes packed very tightly with minimal intergenic space.
  • These are termed "bonsai chromosomes."

Diverse Secondary and Tertiary Groups

• Heterokonts: A large group including diatoms and brown algae that acquired chloroplasts through secondary endosymbiosis of red algae.
• Haptophytes: Marine algae such as Emiliania huxleyi (a marine coccolithophore).
  • E. huxleyi Metabolism: Converts $CO_2$ into organic carbon ($C_6H_{12}O_6$) and inorganic carbon ($CaCO_3$).
  • Prymnesium parvum: Known as golden algae; these form harmful blooms in coastal and inland regions.
• Apicomplexa: This group has retained a non-pigmented plastid known as an apicoplast.
  • The apicoplast has a simple genetic system and is a primary drug target.
  • Antibiotics targeting bacterial RNA polymerase or ribosomes are effective against some apicomplexan species (e.g., malaria parasites).
• Dinoflagellates: Characterized by extreme evolutionary flexibility.
  • Originally likely obtained a red alga chloroplast.
  • $\sim 50\%$ of species discarded the chloroplast to return to heterotrophy.
  • Tertiary Endosymbiosis: Some replaced their original chloroplast with one from a green alga or a haptophyte.
  • Kleptoplastids: Some dinoflagellates maintain temporary chloroplasts stolen from algal prey for several months without replication.

Kleptoplastidy in Animals and Speculation

• Photosynthetic Sea Slugs: Elysia chlorotica is a notable example of a photosynthetic animal.
  • The Process: The slug feeds on the heterokont Vaucheria litorea.
  • Longevity: The slug can survive on sunlight and $CO_2$ for its entire adult life (approximately $9$ months) using stolen chloroplasts.
  • Limitations: The chloroplasts do not divide within the slug and are not transmitted to eggs. Juveniles must feed on Vaucheria to acquire their own.
• Popular Science Speculation: Articles from sources like BBC Future and Scientific American explore the hypothetical question: "What if humans could photosynthesize?" and examine the discovery of solar-powered nourishment in the animal kingdom.