Secondary and Tertiary Endosymbiosis and Kleptoplasty

  • Jeferson Gross
  • Debashish BhattacharyaEmail author
  • Karen N. Pelletreau
  • Mary E. Rumpho
  • Adrian Reyes-Prieto
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 35)


Alga is an informal name that refers to a diverse group of photosynthetic eukaryotes that have a polyphyletic origin in the tree of life. Although genomics has provided powerful tools for understanding the evolution of algal photosynthesis many issues remain unresolved. These include explaining the intermingling of plastid-lacking taxa such as ciliates and oomycetes among plastid-containing groups of chromalveolates. Does this pattern reflect a single ancient endosymbiosis in the chromalveolate ancestor followed by independent plastid losses or multiple secondary endosymbioses? Here we review current knowledge about chromalveolate evolution and phylogeny with a focus on secondary and tertiary endosymbiosis and survey recent genome-wide analyses to assess the potentially broad and lasting impacts of plastid transfer on eukaryote evolution. We assess the evidence for ‘footprints’ of photosynthetic pasts that remain even when the plastid is lost. These data comprise remnant algal genes in the nucleus of plastid-lacking taxa that have putatively originated via intracellular gene transfer from the former endosymbiont. We also provide a survey of recent work done in the field of protein import (i.e., via translocons) into chromalveolate and other plastids derived from secondary endoysmbiosis. We contrast the similarities and differences between primary and secondary plastid protein import machineries and speculate on the key innovations that led to their establishment. And finally, we take a careful look at the remarkable case of sea slug (Elysia chlorotica) kleptoplasty and photosynthesis and review recent work aimed at explaining this phenomenon in different metazoa. In particular, we critically assess support for the hypothesis that sea slug photosynthesis is explained by massive horizontal gene transfer (HGT) from the genome of the captured alga.


Secondary Endosymbiosis Secondary Plastid Primary Plastid Nucleomorph Genome Algal Prey 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



Bipartite topogenic signal


Dry mass


Endoplasmic reticulum associated degradation


Endosymbiotic gene transfer


Endosymbiotic and/or horizontal gene transfer


Endoplasmic reticulum


Horizontal gene transfer


Inner envelope membrane


Microsporine-like amino acids


Marine stramenopile


Outer envelope membrane


Periplastid compartment


Periplastid membrane




RNA-dependent RNA polymerase


Reverse transcriptase


Signal pepide


Stramenopiles Alveolata, Rhizaria


Translocon on the outer/inner envelope of chloroplasts


Tree of life


Transit peptide



This research was partially supported by grants from the National Science Foundation awarded to DB (EF 08-27023, DEB 09-36884, and MCB 09-46528) and to MER (IOS-0726178). MER was also supported by the Maine Agricultural and Forest Experiment Station (ME08361-08MRF, NC 1168). ARP acknowledges support from the Canadian Institute for Advanced Research’s Integrated Microbial Biodiversity Program.


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Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Jeferson Gross
    • 1
  • Debashish Bhattacharya
    • 1
    Email author
  • Karen N. Pelletreau
    • 2
  • Mary E. Rumpho
    • 2
  • Adrian Reyes-Prieto
    • 3
  1. 1.Department of Ecology, Evolution and Natural Resources and Institute of Marine and Coastal SciencesRutgers UniversityNew BrunswickUSA
  2. 2.Department of Molecular and Biomedical SciencesUniversity of MaineOronoUSA
  3. 3.Biology DepartmentUniversity of New BrunswickFrederictonCanada

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