A Secondary Symbiosis in Progress?

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Science  14 Oct 2005:
Vol. 310, Issue 5746, pp. 287
DOI: 10.1126/science.1116125


Algae have acquired plastids by developing an endosymbiotic relationship with either a cyanobacterium (primary endosymbiosis) or other eukaryotic algae (secondary endosymbiosis). We report a protist, which we tentatively refer to as Hatena, that hosts an endosymbiotic green algal partner but inherits it unevenly. The endosymbiosis causes drastic morphological changes to both the symbiont and the host cell architecture. This type of life cycle, in which endosymbiont integration has only partially converted the host from predator to autotroph, may represent an early stage of plastid acquisition through secondary symbiosis.

Endosymbiosis is a major driving force in the evolution and diversification of plants and algae. Plastids originated from a cyanobacterial symbiont harbored in the first eukaryotic algae, of which three “primary algae” are direct descendants: Glaucophyta and Rhodophyta (the red algae) and Viridiplantae (the green algae and land plants). After this primary endosymbiosis, successive secondary endosymbioses occurred in which a primary alga was engulfed and integrated as a plastid. Four algal divisions (Dinophyta, Cryptophyta, Heterokontophyta, and Haptophyta) plus one parasitic phylum (Apicomplexa) acquired red algal plastids, and two algal divisions (Chlorarachniophyta and Euglenophyta) acquired green algal plastids (1).

Endosymbiosis unites different cells into one organism. Requisite steps include a lateral gene transfer from the symbiont to the host nucleus and the establishment of protein transport machinery back into the symbiont, resulting in loss of the symbiont's autonomy (2). Synchronization of host-symbiont cell cycles and cosegregation is another critical step in permanent fusion of the two partners. However, how the synchronization occurs and how the integrated organism responds to external conditions are unknown.

Here we describe a flagellate (Fig. 1A) that appears to be in the formative stages of an ongoing endosymbiosis. The flagellate, which we tentatively refer to as Hatena (“enigmatic” in Japanese), will be formally described as a member of a recently elected division Katablepharidophyta (3). Hatena is currently uncultivable, so cells from natural populations were used for investigations. Nearly all the cells had a green “plastid” with an eyespot at the cell apex. However, this plastid was inherited by only one daughter cell (Fig. 1B), indicating the structure is a symbiont.

Fig. 1.

(A) Hatena (ventral view). All green, symbiont-possessing cells have an eyespot at the cell apex (arrowhead). Scale bar, 10 μm. (B) A dividing cell (ventral view). The symbiont is always inherited by only one of the daughter cells. Scale bar, 10 μm. (C) The ultrastructure of eyespot integration (longitudinal view). E, eyespot granules. Scale bar, 400 nm. Inset: A magnified view of the membranes. The inner and outer plastid membranes (arrowheads), the single symbiont-enveloping membrane (double arrow), and the host plasma membrane (arrow) are tightly layered. Scale bar, 50 nm. (D) The life cycle of Hatena, based on observations of natural populations. Hatena alternates between a host phase that harbors a green endosymbiont and a predator phase that acquires the endosymbiont after division. Solid line, observed steps in the process; broken line, hypothetical steps.

We determined the identity of the endosymbiont by sequencing of the plastid 16S ribosomal DNA (rDNA) and by phylogenetic analysis. The symbiont belongs to the genus Nephroselmis (Prasinophyceae, Viridiplantae) (fig. S1), which is abundant in the habitat.

The symbiont cell retains its nucleus, mitochondria(on), plastid, and occasionally a vestigial Golgi body, but the flagella, cytoskeleton, and endomembrane system are lost. Free-living Nephroselmis cells are flat-kidney-shaped, are ∼10 μm in length, and possess a single plastid with a single pyrenoid (4). In contrast, the symbiont's plastid is more than 10 times as large (Fig. 1A) and contains multiple pyrenoids.

Ultrastructure also indicates remarkably close interaction between the host-symbiont partnership. An eyespot (located in the endosymbiont's plastid) is always situated at the host's apex (Fig. 1A, arrowhead), where four membranes (the inner and outer plastid membranes, the symbiont-enveloping membrane, and the host's plasma membrane) are tightly apposed (Fig. 1C). The eyespot is part of a photosensor that enables phototaxis (5). Intimate morphological association between the endosymbiont and the host indicates endosymbiont-guided host phototaxis.

The corresponding region in the colorless, symbiont-lacking cells is occupied by a complex feeding apparatus. Thus, the uptake of the symbiont also induces drastic changes to the host cell. We tested the specificity of the host-symbiont interaction by feeding symbiont-free hosts with a different Nephroselmis strain (one with 31 out of 335 base pairs different, according to partial 16S rDNA sequencing). Although the prey was engulfed and remained undigested, it did not undergo the modifications described above, suggesting a highly strain-specific interaction.

The Hatena life cycle thus alternates from a predator phase to an autotrophic host phase (Fig. 1D). First, a green cell (step a) divides (b) into one green (c) and one colorless (d) cell. The colorless cell develops a feeding apparatus de novo (d to e) and engulfs a Nephroselmis (e to g). The symbiont plastid develops and the feeding apparatus degenerates (g to a). As we never observed any dividing cell without a symbiont (d) or with an “immature” plastid (h), symbiont acquisition and modification apparently occur within one generation. How many generations the symbiont persists is an open question.

Hatena represents an early stage in the development of an ongoing secondary endosymbiosis. Some dinoflagellates are also known to be in the process of acquiring symbionts (6). However, past research has been focused only on symbiont changes. Hatena demonstrates changes in both host and symbiont. It now remains to be determined whether there has been lateral gene transfer between Hatena and its Nephroselmis symbiont, as such genetic amalgamation was a key step in the evolution of modern plants and algae.

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