Metabolic Symbiosis and the Birth of the Plant Kingdom

Abstract

Eukaryotic cells are composed of a variety of membrane-bound organelles that are thought to derive from symbiotic associations involving bacteria, archaea, or other eukaryotes. In addition to acquiring the plastid, all Archaeplastida and some of their endosymbiotic derivatives can be distinguished from other organisms by the fact that they accumulate starch, a semicrystalline-storage polysaccharide distantly related to glycogen and never found elsewhere. We now provide the first evidence for the existence of starch in a particular species of single-cell diazotrophic cyanobacterium. We provide evidence for the existence in the eukaryotic host cell at the time of primary endosymbiosis of an uridine diphosphoglucose (UDP-glucose)-based pathway similar to that characterized in amoebas. Because of the monophyletic origin of plants, we can define the genetic makeup of the Archaeplastida ancestor with respect to storage polysaccharide metabolism. The most likely enzyme-partitioning scenario between the plastid's ancestor and its eukaryotic host immediately suggests the precise nature of the ancient metabolic symbiotic relationship. The latter consisted in the export of adenosine diphosphoglucose (ADP-glucose) from the cyanobiont in exchange for the import of reduced nitrogen from the host. We further speculate that the monophyletic origin of plastids may lie in an organism with close relatedness to present-day group V cyanobacteria.

Dating the cyanobacterial ancestor of the chloroplast

“…Tomitani et al 1 suggested, on the basis of genetic distances and fossil calibrations, an age ranging from 2450 to 2100 MYA for heterocyst forming cyanobacteria, predating the rise of atmospheric oxygen to around 2300 MYA. Recently, Deschamps et al 12 provided the first evidence of the existence of starch in bacteria within unicellular, N 2 fixing cyanobacteria, belonging to Order Chroococcales. These authors suggested that starch formation would define the genetic make-up of the ancestor of the plant kingdom related to storage polysaccharide metabolism.…”

“…The above suggests that the ancestor of chloroplasts had the ability to fix N 2 , fix CO 2 by an oxygen-evolving II-type photosystem, and store starch. The ancient symbiosis metabolic fluxes consisted of the export of ADP-glucose from the cyanobiont to the host, eliminating its ability to store polysaccharides, thus in habilitating its capacity to fuel N 2 fixation, demanding the import of reduced nitrogen from the host to the cyanobiont 12 .…”

Convergent Evolution of Polysaccharide Debranching Defines a Common Mechanism for Starch Accumulation in Cyanobacteria and Plants

“…Until recently, the distribution of starch seemed restricted to photosynthetic eukaryotes, including several secondary endosymbiosis lineages derived from Archaeplastida, such as the cryptophytes (Deschamps et al, 2006), the dinoflagellates (Dauvillée et al, 2009), and some apicomplexa parasites (Coppin et al, 2005). However, more recent studies revealed the existence of starch-like structures in unicellular diazotrophic cyanobacteria belonging to the order Chroococcales (Nakamura et al, 2005;Deschamps et al, 2008;Suzuki et al, 2013). The presence of anomalous glycogen particles had already been identified previously in this clade, while it is only very recently that this material was recognized as starch-like and the term "semiamylopectin" was coined to describe the major amylopectin-like fraction within these granules (Schneegurt et al, 1994;Suzuki et al, 2013).…”

“…Four out of the six reported starch-accumulating cyanobacteria strains accumulate only this polysaccharide fraction. However, two different strains also synthesize amylose using an enzyme phylogenetically related to the archaeplastidial granulebound starch synthase (GBSS), an enzyme known to be selectively responsible for the synthesis of this fraction in plants (Delrue et al, 1992;Deschamps et al, 2008).…”

Quantitative Assay Method for Starch Branching Enzyme with Bicinchoninic Acid by Measuring the Reducing Terminals of Glucans

“…These specific features of amylopectin fine structure are enabled by the localization of position of branches in the cluster. 6) The starch synthesis system has developed during the process of evolution of plants, 6,7) and key enzymes involved in the construction of amylopectin tandem cluster structure have differentiated into multiple isozymes with distinct functions whereas in glycogen synthesizing organisms such as bacteria and animals no such functional differentiations in glycogen synthesis enzymes have occurred. 8,9) Starch branching enzyme (BE) plays an important part in the formation of branches in amylopectin molecules.…”