What is the significance of the ubiquity of chlorophyll a

For instanse, such risk must be critical particularly upon dynamic cellular interactions that potentially disrupt the mechanisms quenching photoexcited chlorophylls in the phototrophic cells. Extensive examination of a wide variety of phagotrophic, parasitic, and phototrophic microeukaryotes demonstrates that a catabolic process that converts chlorophylls into non-photosensitive ,cyclopheophorbide enols CPEs is phylogenetically ubiquitous among extant eukaryotes. CPE catabolism is identified in phagotrophic algivores belonging to virtually all major eukaryotic assemblages with the exception of Archaeplastida, in which no algivorous species have been reported.

In addition, CPE catabolism is revealed to be common among phototrophic microeukaryotes i. Thus, it is implied that CPE catabolism primarily evolved among algivorous microeukaryotes to detoxify chlorophylls in an early stage of their evolution. Chlorophylls are essential components of the photosynthetic apparati that sustain all of the life forms that ultimately depend on solar energy.

However, a drawback of the extraordinary photosensitizing efficiency of certain chlorophyll species is their ability to generate harmful singlet oxygen. Each of these MEAs includes phototrophic groups, namely dinophytes, haptophytes, ochrophytes, and cryptophytes phototrophic cryptomonads , respectively.

Their secondary and tertiary chloroplasts derived from a red alga were acquired independently in each clade [ 26 ]. It is noteworthy that the production of CPEs has associated with the digestion of algae in an algivorous dinoflagellate Amphidinium sp.

This seems to be analogous to the chloroplast dismantling seen in euglenophytes. S2C [ 27 ]. CACC was also previously reported in the dinoflagellate Noctiluca scintillans , grown in heterotrophic conditions [ 12 ].

Ciliates are also potential CPE producers in aquatic environments because many of them are able to consume microalgae. Goericke et al. However, CACC seems to occur sporadically among ciliates. From the six species of algivorous and mixotrophic ciliates we tested, only Frontonia sp. Formation of brown globules in cells was typically observed in aged cultures of the strains that exhibited CACC Fig.

Haptophytes are a monophyletic group of algae within the MEA Haptista, hence nested within heterotrophic microeukaryotes [ 26 ] Supplementary Fig.

Importantly, as reported here and in previous studies, CACC is generally present among the Centroplasthelida centrohelids , a basal group of Haptista representing the heterotrophs Supplementary Fig. An intriguing absence of CACC in UCs was found among ochrophytes and cryptophytes, even if their chloroplasts are derived from a red alga similarly to dinophytes and haptophytes. In TCs, however, many of algivorous Stramenopiles exhibited CACC upon predation of algae, which include some of mixotrophic species of ochrophytes i.

Furthermore, CPE production was commonly observed among algivorous Cryptista, including three Cyano-TCs of cyathomonadaceans goniomonads and two TCs of katablepharids that prey on algae Fig. S2E and Supplementary Table S2. All strains we tested in Amoebozoa and Opisthokonta were algivores in TCs because no phototroph has been discovered among these MEAs [ 16 ].

Accumulation of CPEs was observed in a half of the Amoebozoa species examined in the present study. CACC was clearly detected in an algivorous strain of Neoparamoeba sp. Among the Opisthokonta species, we found CACC only among the chytrid fungi, when parasitizing diatoms. The discovery that eukaryotic algae with secondary chloroplasts produce CPEs under photoautotrophic culture conditions extends our understanding of microeukaryotic chlorophyll catabolism beyond algivory.

Our microscopic observations suggest that the algal CPE accumulation occurs in association with the dismantling of chloroplasts in parallel with formation of brownish, nonfluorescent globules observed in chlorarachniophytes, euglenophytes, and haptophytes. This indicates a role for the algal CACC in controlled chloroplast degradation. We infer that the CACC observed in each of these four lineages of algae was inherited from phagotrophic ancestors, rather than derived from the green or red algal progenitors of their secondary chloroplasts.

For example, because all the algivorous euglenozoan examined clearly displayed accumulation of CPEs during the digestion of algae Fig. Because euglenophytes are monophyletic within Euglenozoa [ 24 ], algal CACC is most likely have descended from an ancestral euglenozoan host cell. Similarly, we suggest that the CACC of chlorarachniophytes, haptophytes, and dinophytes is also likely descended from their phagotrophic ancestors.

In these cases, the metabolic strategy originally used to accommodate the phototoxicity of dietary chlorophylls also allowed for the retention of phagocytosed algae as endosymbionts, and thus facilitated their evolution as secondary chloroplasts. A secure biochemical strategy for the degradation of chlorophylls, such as CACC, must have been essential for microeukaryotes that occasionally dismantled their chloroplasts.

In addition to the CACC associated with chloroplast dismantling, accumulations of CPEs were also observed in some two-membered algal co-cultures, where one alga mixotrophically preys on the other.

In particular, a strain of chrysophycean alga Poterioochromonas malhamensis exhibited quantitative accumulation of CPEs along with preying on the green alga Chlamydomonas , where accumulation of cPPB- b E, chlorophyll- b -derived CPEs can be only explained by catabolic conversion of chlorophyll b produced in Chlamydomonas by the chrysophycean. Such mixotrophy has also been known among those algae with secondary chloroplasts including chrysophyceans ochrophytes , haptophytes, dinophytes, and cryptophytes [ 28 ].

Although it has not been thoroughly checked, the apparent absence of CACC in some of the UCs including those of cryptophytes may not reflect the lack of CACC at all, since we have not examined then under culture conditions as Cyano-TC. Obviously, therefore, investigation of CACC among algivorous mixotrophs is an important topic for future research.

That CACC among secondary phototrophs is derived from phagotrophic ancestors is supported by the consistent absence of CPEs among the green and red algae Chloroplastida and Rhodophyceae, respectively; Fig. In fact, Archaeplastida does not exhibit accumulation of CPEs.

However, it is unclear whether the phagotrophic ancestor of Archaeplastida which acquired a cyanobacterial symbiont by phagocytosis was a CPE producer, because phagocytosis is very unusual in extant Archaeplastida, with very few exceptions mixotrophic green algae, such as Cymbomonas [ 29 ].

Nonetheless, Archaeplastida also requires a catabolic strategy to detoxify chlorophylls when attempting oxygenic photosynthesis, although this strategy might differ from the CACC. Among archaeplastids, land plants are known to catabolize chlorophylls into colorless and nonphototoxic catabolites [ 30 , 31 ]. Sequences homologous to the PAO gene have been widely identified among the Chloroplastida and cyanobacteria, as well as other algae with secondary chloroplasts [ 32 ].

Although a similar function has not yet been identified for these homologs, the apparent lack of CACC in some of these organisms indicates that they may degrade chlorophyll to nonphototoxic colorless products e. Associated with this study, for example, Palpitomonas bilix , the most basal lineage of Cryptista Supplementary Fig. Furthermore, the green color of the chloroplasts of the pedinophycean rapidly faded to transparency under microscopic observation Fig.

Therefore, the endosymbiosis of a cyanobacterium by the common ancestor of Archaeplastida, which gave rise to chloroplasts, might have been facilitated by a detoxification strategy other than the CPE accumulation.

The observed phylogenetic ubiquity of CACC among eukaryotes strongly indicates that the acquisition of CACC was a key evolutionary step that led to the diversity of extant eukaryotes. A typical example illustrating this can be found in the Rhizaria, in which accumulation of CPEs was detected in all 12 algivorous strains representing 9 distinct lineages and in all 12 phototrophic strains chlorarachniophytes , encompassing the full rhizarian diversity.

Importantly, the evidence of CACC in Retaria demonstrates both its ecological and paleoecological significance through time. Furthermore, these microeukaryotes form mineral skeletons or tests, which allows their preservation to be reliable fossil evidence.

Many fossil occurrences of these organisms, which date back to the early Cambrian Period [ 34 , 35 ] or earlier [ 36 ], support the consistent importance of the rhizarian heterotrophs, which constituted the primary consumers in the marine food web throughout the Phanerozoic.

The strong conservation of CACC in this taxon suggests the broad importance of algivory in the evolution of the Rhizaria. Why does CACC occur so widely among eukaryotes? The wide occurrence of CACC reflects the fact that managing the phototoxicity of chlorophylls is crucial to any organism living in an illuminated, oxygenated environment and in close contact with chlorophyll-dependent photosynthesis.

The consistent observation of CACC in particular clades e. Another hypothesis is that CACC have been acquired several times in the early stage of eukaryote radiation; in such a case, CACC may have been spread horizontally by horizontal gene transfer, or acquired independently several times through the course of evolution. Unfortunately, however, precise reconstruction of the evolutionary history of CACC is currently difficult because the genetic basis for CACC still remains unknown.

Convincing examples are found in Rhizaria and Euglenozoa, and imply the universal occurrence of CACC, because the origins of these groups have been dated to the late Mesoproterozoic ca. Therefore, CACC is estimated to have been acquired by eukaryotes before the last Snowball Earth event, and before the increase in global p O 2.

Comparative reconstruction of the temporal evolution of atmospheric p O 2 and estimated age of emergences of major eukaryotic assemblages MEAs. The yellow and green lines delineate the upper and lower limits, respectively, of the estimated range based on geochemical proxies [ 3 ]. Red arrow on the top indicates the time point 0. This illustrates a conspicuous discrepancy between the timing of the final oxygenation of the atmosphere and the appearance of extant eukaryotic lineages with notable affinity for molecular oxygen.

The evolution of algivores equipped with CACC must have been an ecological breakthrough in the history of the eukaryotes. This explanation is consistent with the origin of mitochondrial respiration, which can also be traced back at least to LECA Fig. CACC subsequently allowed the direct and massive in situ consumption i.

Thus, the ecological advantage conferred by CACC exapted extant eukaryotic lineages to the dramatic biogeochemical changes in primary production that led to the increase in global p O 2 , and together with the physiological advantages conferred by mitochondria, allowed their construction of, and successful radiation into, the fully oxygenated Earth to the present day. Ocean oxygenation in the wake of the Marinoan glaciation.

Low mid-proterozoic atmospheric oxygen levels and the delayed rise of animals. Gray MW. DOI: Kashiyama , A. Tamiaki Published 4 September Biology, Medicine Proceedings of the National Academy of Sciences Chlorophylls are essential components of the photosynthetic apparati that sustain all of the life forms that ultimately depend on solar energy.

However, a drawback of the extraordinary photosensitizing efficiency of certain chlorophyll species is their ability to generate harmful singlet oxygen. Recent studies have clarified the catabolic processes involved in the detoxification of chlorophylls in land plants, but little is understood about these strategies in aquatic ecosystem. Here, we report… Expand. View on NAS.

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