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Earth-Sci Rev — Food Chem Toxicol — Annals of botany 5 — Reality and perspectives. The older 1. Thus, although Obruchevella is a probable cyanobacteria, these hypotheses are only based on morphology and size, and would be strengthened by ultrastructure and chemical analyzes.
Oscillatoriacean cyanobacteria are reported as the most represented group of cyanobacteria in the fossil record [ ]. Oscillatoriopsis microfossils are slightly constricted at intercellular septa [ ]. Oscillatoriopsis microfossils are commonly found in shallow water marine environments but they also may be found in lacustrine deposits or pluvial lakes [ 50 , , ].
The stratigraphic record of this genus starts with the ca. The interpretation is only based on morphology, similar to modern Oscillatoria. However, this type of simple morphology is also found among other prokaryotes such as Beggiatoa , a sulfide-oxidizing proteobacterium [ 41 , 50 , , ] or among eukaryotes such as Ulothrix , a green alga [ ]. Oscillatoriacean cyanobacteria often reproduce by the formation of hormogonia. The fossil occurrence of such short filamentous microfossils interpreted as Oscillatoriopsis could support its identificationas hormogonia of oscillatoriacean cyanobacteria [ ].
However, other bacteria, again including Beggiatoa , may also produce hormogonia. Therefore, the interpretation of Oscillatoriopsis as an oscillatoriacean cyanobacterium, albeit plausible, is still debated [ 41 ]. Palaeolyngbya is interpreted as a hormogonian oscillatoriocean cyanobacterium microfossil found first in the 0. It is a sheathed filament with a smooth wall Fig.
Regular and uniseriate discoidal cells are arranged inside the single sheath [ ]. As several other possible cyanobacteria microfossils, Palaeolyngbya has been interpreted as such based only on its morphology [ , ] and therefore is debatable. Polysphaeroides is a fossil genus described by Hermann [ ], which included several fossil species, until , when Hofmann and Jackson [ ] moved nearly all of the species of Polysphaeroides to the genus Chlorogloeaopsis , because of their similar morphology.
Only one species remained, Polysphaeroides filiformis [ ]. Polysphaeroides filiformis consists of spheroidal cells arranged in a loose multiseriate filamentous aggregate and surrounded by a common envelope with closed ends Fig.
The colonies formed by the spheroidal cells may branch. The 1. Polysphaeroides is compared to modern stigonemataleans [ , ], although some authors suggested a possible affinity to eukaryotic algae, either green or red [ ], for example the red algae Polysiphonia Figs.
However, the morphology of Polysphaeroides filiformis, characterized by a thick sheath surrounding multiseriate filament arrangement and occasional branching, fits the description of the recently re-evaluated modern genus Stigonema [ ].
For instance, Polysphaeroides filiformis from the 1. We consider that this fossil cyanobacterium may represent a good alternative calibration for future molecular clock analyses as modern taxa belonging to this genus form a monophyletic clade.
Modern multiseriate Stigonema species including the recently described S. Siphonophycus is one of the most common filamentous microfossils in the Proterozoic. It is commonly found in shallow water deposits in Proterozoic mat assemblages [ 41 , ], preserved in situ in chert [ 41 , 80 , , , ] or as bundles ripped off mats in shales [ 54 ], or as the main stromatolite builders [ 50 ].
Siphonophycus is an unbranched, non-septate and empty smooth-walled filamentous sheath [ ] Fig. Several species are distinguished based on the diameter range of the filamentous sheath [ ].
Similar Oscillatoriales-like microfossils occur through all the Proterozoic. Siphonophycus specimens are generally interpreted as sheaths of oscillatoriacean cyanobacteria.
Schopf [ ] occasionally observed transverse thickenings that were placed along Siphonophycus filamentous sheaths. Therefore, he suggested that modern counterparts of Siphonophycus microfossils would be LPP-like cyanobacteria Lyngbya , Phormidium and Plectonema [ , , ]. Nevertheless, this simple morphology is also encountered in other bacteria. For example, minute Siphonophycus sheaths may be comparable to Chloroflexi -like photosynthetic bacteria [ 41 , ].
Large Siphonophycus microfossils might also be the remains of filamentous eukaryotic algae [ 50 ]. Thick sheaths are generally common among cyanobacteria and not among other bacterial phyla [ ].
They may thus be a criterion of a cyanobacterial affinity for those Siphonophycus specimens, in addition to alternating vertical and horizontal disposition in mats, which may indicate phototropism or chemotropism, a behavior not unique to cyanobacteria [ 41 , ].
The understanding of cyanobacterial phylum evolution has progressed significantly with the emergence of molecular biology techniques and new sequencing technologies. Since the late 90's a myriad of phylogenetic studies based on single loci i. Even if the five major sections of Cyanobacteria were not yet represented in genomic databases, the first studies to use a phylogenomic i.
In , the large CyanoGEBA Genomic Encyclopedia of Bacteria and Archaea sequencing project led to an improvement in terms of genomic coverage of cyanobacterial taxa, notably by sequencing genomes belonging to sections II and V [ ]. Since then, the number of publicly available cyanobacterial genomes has dramatically increased.
Yet, their quality, especially contamination of cyanobacterial assemblies by non-cyanobacterial DNA, has gone worse in parallel, which is a problem for phylogenetic analyses [ ]. Moreover, the real biodiversity of cyanobacteria is still under-represented in genomic databases, mainly because of a biased sampling in the sequencing effort [ , ].
Nevertheless, since Shih et al. Most of these studies focussed on integrating new genomic data to the same set of — hundreds loci but see Ref. By doing so, few tried to handle the methodological difficulties associated with the use of large-scale data to resolve the phylogeny of old groups such as Cyanobacteria, whether during dataset assembly e. Consequently, among the ten phylogenomic studies cited above, only three are in agreement on the cyanobacterial backbone [ 13 , , ].
For molecular clock reconstructions, microfossils of cyanobacteria are needed as a source of calibration of the molecular phylogenies. However, only few calibration points are available to date oxygenic photosynthesis, the endosymbiotic event having given rise to the chloroplast, as well as the origin of cyanobacteria.
Beyond the lack of congruence of the phylogenomic studies and the polyphyletic nature of many cyanobacterial groups including well-known genera such as Synechoccocus and Leptolyngbya , the issue is complicated by the absence in genomic databases of modern counterparts Entophysalis , Hyella or Cyanostylon -like of the unambiguous cyanobacteria microfossils Eoentophysalis , Eohyella and Polybessurus.
As we have no reliable indication of the phylogenetic position of these important modern taxa, researchers often use flimsy affiliations as calibration points.
Usually, only few cyanobacterial fossils are used as constraints for molecular clock analyses. They include Archaeoellipsoides for monophyletic Nostocales and Stigonematales lineages, and Eohyella for Pleurocapsales lineages, despite the absence of a genetic characterization of the modern counterpart Hyella e. The occurrence of fossil diatoms is often used for the advent of the endosymbiont Rivularia intracellularis, and the fossil red algae Bangiomorpha for the minimum age of the primary endosymbiosis.
Moreover, some authors have chosen not to use cyanobacteria microfossils in their analysis, but instead fossils from eukaryotic lineages such as plants [ ], or the occurrence of horizontal gene transfer [ ], or the GOE to set a lower bound on Cyanobacteria as a phylum [ ]. In a non-exhaustive survey, we observed more than 89 different approaches used to estimate the evolution of cyanobacterial phylum.
This diversity of phylogenies, and calibration points, but also of clock models and dating software packages, has led to a large variety of age estimates.
Microfossils record of unambiguous, probable and possible cyanobacteria see text for discussion, Table 1 , and Supplementary Table 1 , and of Bangiomorpha as an unambiguous red alga, and minimum median age estimates for the divergence of sections I, II, III, IV and V as described by Rippka et al.
Note that the age of Polysphaeroides filiformis considered here corresponds to its record in Baludikay et al. So far, all the attempts to date the evolutionary events of the cyanobacterial phylum used a fixed-node approach, where researchers manually select nodes to place calibration points. The affiliation error is often due to misleading morphological similarities between unrelated extant organisms and ambiguous microfossils.
Moreover, polyphyletic groups make impossible to specify node calibrations, except by reporting their origin to a much older common ancestor far back in the tree.
This problem could be even worse if some scarcely sampled extant organisms used for calibration are actually polyphyletic. Regarding ages, they are specified as prior distributions partly based on the minimum age lower bound or oldest occurrence of a given microfossil in the paleontological record. However, owing to issues due to taphonomy and extinction of stem groups, this may introduce an unmeasurable divergence between the ages specified for the fossil and the real geological span of the organism.
Ultimately, inferred node ages are thus highly dependent on the completeness of the paleontological record [ ]. Because of these limitations, an alternative strategy, termed tip-dating, would be more suitable for dating the evolution of Cyanobacteria.
In such an approach, the placement of the microfossils within the tree is guided by a morphological matrix and supported by statistical values, the posterior probabilities [ ]. Further, by explicitly modeling stem groups within the tree [ ], tip-dating is able to test and thus either confirm or reject the affiliation of microfossils to extant organisms, which is usually taken for granted in the paleontological literature and many molecular dating studies building upon it.
In most cyanobacterial phylogenetic analyses that are using a non-cyanobacterial outgroup to root the tree, the reference strain Gloeobacter violaceus PCC has a basal position [ 9 , [] , [] , [] ]. Consequently, the phylogenetic node bearing Gloeobacter and the rest of modern cyanobacterial lineages serves as calibration for the origin of cyanobacteria in several studies [ [] , [] , [] ].
In these studies, the authors have set different root limit ages, so that the maximum root age may vary between the earliest estimate of abiogenesis around 4. Recently, two newly discovered lineages were proposed as sister groups of the cyanobacterial phylum, the Melainabacteria [ ] and the Sericytochromatia [ ].
Of note, these lineages mostly known as metagenomics assemblies do not contain genes required for photosynthesis nor carbon fixation [ ]. The integration of genetic data from Melainabacteria and Sericytochromatia as outgroups for molecular clock analyses suggested that cyanobacteria evolved just before the GOE [ , ]. Taken together, this suggests that oxygenic photosynthesis has evolved after the separation of cyanobacteria from Melainabacteria [ , ].
However, the loss of photosynthetic capability in the ancestor of the three lineages before or at the time of GOE has been suggested as an alternative hypothesis that cannot be ruled out [ ]. Among bacterial phototrophs cyanobacteria, green S-bacteria, green non sulfur bacteria, purple bacteria, heliobacteria, some acidobacteria and gemmatimonadetes , Cyanobacteria is the only lineage that possesses two photosynthetic reaction centers of the Fe—S type RCI and Quinone type RCII , whereas anoxygenic bacteria possess either the Fe—S or Quinone type.
So far, three hypotheses were proposed to explain the presence of both types of RC in modern cyanobacteria. Two of these hypotheses suggest that both RCs would have been present in an anoxygenic phototrophic ancestor. In a first hypothesis, RCs evolved within the common ancestor of all bacterial phototrophs.
Both of them were kept in the cyanobacterial lineage whereas there was a selective loss of one type of each in the modern anoxygenic lineage ancestors [ , ]. This was followed by lateral transfer of a different RC type to the ancestors of the modern anoxygenic phototrophs [ ]. The existence of an anoxygenic cyanobacterial ancestor may be supported by the occurrence of several genes involved in anoxygenic photosynthesis in modern cyanobacterial genomes [ ], and the co-occurrence of both anoxygenic and oxygenic photosynthesis in several lineages of modern cyanobacteria clades [ , ].
A third hypothesis rather suggests the independent evolution of the two RCs in separate lineages of anoxygenic phototrophs and their lateral transfer into a protocyanobacterial ancestor, the so-called fusion hypothesis [ , ].
This observation makes the transfer of full photosystems highly plausible, and recent events of such kind have been convincingly inferred in Rhodobacteraceae [ ]. In order to test the likelihood of the ancient transfer of photosystems between the bacterial phototrophic lineages, Magnabosco and colleagues [ ] added horizontal gene transfer events information of two genes encoding for Mg-chelatase and S-adenosyl- l -homocysteine hydrolase as additional constraints to their models to estimate the stem age of the bacterial phototrophs Cyanobacteria, green S-bacteria and green non-sulfur bacteria.
These authors assumed that such estimates would allow them to investigate the feasibility and timing of the RC transfer events between phototrophic lineages. Their results excluded the possibility of a RC transfer from the green sulfur bacteria to cyanobacteria, and thus, invalidated the fusion hypothesis.
However, they were not able to choose between the two hypotheses suggesting that both RCs emerged from a common ancestor [ ]. First, the reaction centers RCI and RCII would operate separately and asynchronously in the same ancestral anoxygenic phototroph organism.
However, the evolution of these processes, and the early or late evolution of oxygenic photosynthesis, are still debated e. Several studies suggested that ancestral cyanobacteria first inhabited freshwater ecosystems [ 13 , 15 , 17 , , , ], but see e.
Nevertheless, these estimates are based on comparison with the modern ecology of basal clades of cyanobacteria, which are likely to have changed through time. Moreover, the fossil record of cyanobacteria is almost exclusively estuarine and shallow marine, often from the intertidal zone, or hypersaline lacustrine. However, terrestrial deposits are less commonly preserved in the geological record, and this might bias our view of the fossil ecological ranges.
A couple time calibrated phylogenies based on low-resolution alignments of 16S rRNA gene sequences or on a large multilocus dataset [ , ] suggest that multicellular forms of cyanobacteria were potentially present when the GOE started, implying a pre-GOE origin of the cyanobacterial phylum.
Furthermore, their results hint at an acceleration of the diversification rate after the substantial increase of atmospheric oxygen concentration [ ]. The acquisition of the multicellularity would be an advantage for UV resistance and substrate adhesion [ 40 ]. However, multicellularity is polyphyletic and convergent several times across extant species — especially in cyanobacteria. Other studies hypothesize that the origin of marine planktonic cyanobacteria would have happened after the evolution of crown groups in freshwater, terrestrial and benthic coastal modern environments [ ].
Benthic terrestrial and coastal cyanobacteria may have dominated the oxygenic photosynthesis from the late Archean and possibly until the mid-Neoproterozoic [ ]. However, these hypotheses remain to be confirmed since the record of Archean cyanobacteria is controversial as explained above, and the fossil record is biased towards benthic forms.
Benthic filamentous cyanobacteria forming mats or preserved in silicified stromatolites are preserved preferentially to small planktonic cells sedimenting in the water column. Moreover shallow-water deposits are more common in the Precambrian then deeper sediments.
Non-heterocytous N-fixing unicellular and filamentous Trichodesmium spp. This observation possibly coincides with an increase of bioavailable Mo an essential co-factor of nitrogenase in the open ocean [ 40 , , , ]. However, cyanobacteria likely had to invent a new N 2 -fixation machinery that could operate in the presence of the rising O 2 , leading to the evolution of heterocytous cyanobacterial taxa, probably as early as the GOE [ ], and possibly supported by Paleoproterozoic [ [] , [] , [] ] and Neoproterozoic [ ] microfossils.
However, this hypothesis might be questioned as heterocytous cyanobacteria age estimates resulted from models that used poorly preserved putative fossil akinetes from 2. However, they became important primary producers in the still stratified mid-Proterozoic oceans [ 38 ].
Chloroplasts form a monophyletic cluster within the Cyanobacteria phylum [ 12 ]. This observation is elegantly interpreted as the result of a primary endosymbiosis at the origin of the chloroplast [ ]. Although this theory is well accepted in the scientific community but see Ref. Two major scenarios are opposed, one postulating an ancient origin early-branching [ 13 , 14 , , , , , , ] and the other one postulating a relatively recent late-branching origin [ 12 , , ].
The hypothesis of an early origin is more frequent in the literature, and it has recently been strengthened by the study of Ponce-Toledo et al. However the calibration used included Archean ages for the highly controversial Apex chert microstructures and sterane that were subsequently reassessed as contaminants see above.
Later studies of ATP synthases subunits and elongation factors permitted to estimate the first endosymbiosis event at approximately 0. Taking advantage of the recent discovery of Gloeomargarita [ 13 , ], Sanchez-Baraccaldo et al.
This result is similar to the one reported in Ref. In contrast, Shih et al. Interestingly, this latter estimate is more similar to the result of [ 12 ], even if assuming an early-branching hypothesis for plastid emergence. Indeed, if differences do exist in tree topologies concerning chloroplast emergence, the wide age intervals obtained in the various analyses often exceed the branch length variation implied by topological changes.
This is not surprising given the very short length of the corresponding internodes in the cyanobacterial backbone. As exploitable cyanobacterial microfossils are not numerous, a logical strategy is to use the morphologically more complex and more recent eukaryotic algae as calibration points. However, the oldest unambiguous fossil record of eukaryotic algae are silicified multicellular bangiophyte red algae preserved in hypersaline shallow-water environment [ ] and recently well dated at 1.
These fossils were interpreted as benthic multicellular red algae based on their morphology, longitudinal division pattern, attachment structures, and ecology [ ]. Other 1. Microfossils interpreted as green algae may also provide an estimation of the minimum age for chloroplast acquisition. Their fossil record ranges from unambiguous 0. Using the new age of 1.
Cyanobacterial fossil record starts unambiguously at 1. Eoentophysalis, Polybessurus and Eohyella microfossils present a combination of distinctive morphologies, modes of division and ecology that are diagnostic of the cyanobacteria phylum [ 41 ]. Therefore, their placement into this phylum is strongly supported, unlike other Proterozoic microfossils that display a simpler morphology widespread among other prokaryotes.
Older possible geochemical traces of oxygenation and the metabolisms involved in stromatolites and MISS builders in the Archean are discussed. Moreover, the origin and timing of oxygenic photosynthesis is also still debated although some studies corroborate that the evolution of oxygenic photosynthesis happened right before the GOE which would then be a consequence of this evolution.
The origin, timing and environment of the primary endosymbiotic event giving rise to eukaryotic algae are also still debated. Therefore, it is essential to define new biosignatures indicative of cyanobacteria in order to reassess their fossil record and provide new calibration points for molecular clocks.
Those biosignatures will combine analyses of the morphology, ultrastructure and ecology of promising microfossils identified in this review, with their molecular lipids and pigments , metal and isotopic composition. Identifying these fossils, not only as cyanobacteria, but of specific clades within the cyanobacteria, will improve our understanding of their diversification record and provide new calibration points.
Coupling these new microfossil calibration points with improved molecular phylogenies and alternative molecular clocks such as tip-dating will then enable to date the minimum ages of important biological events such as the origin of oxygenic photosynthesis and the acquisition of chloroplasts among photosynthetic eukaryotic lineages. We thank the editors W. We also thank Prof.
Knoll, Dr T. Hauer, Dr B. Baludikay and J. Beghin for providing pictures to illustrate this review. Finally, we also thank anonymous reviewers for their insights and comments. National Center for Biotechnology Information , U. Sponsored Document from.
Free Radic Biol Med. Catherine F. Javaux a. Yannick J. Emmanuelle J. Author information Article notes Copyright and License information Disclaimer.
Demoulin: eb. This article has been cited by other articles in PMC. Associated Data Supplementary Materials Multimedia component 1. Abstract Cyanobacteria played an important role in the evolution of Early Earth and the biosphere.
Graphical abstract. Open in a separate window. Introduction Modern cyanobacteria constitute an ancient and well-diversified bacterial phylum, with unique complex morphologies and cellular differentiation.
Fundamental and unresolved questions regarding the early evolution of cyanobacteria What are the timing, pattern, and environment of cyanobacteria origin and evolution? How to interpret the discrepancies between the fossil record and molecular phylogenies, and how to reconcile these records? What are the origin and timing of oxygenic photosynthesis? Which among geochemical redox proxies and stromatolites are reliable indicators of oxygenic photosynthesis?
What is the origin, timing, and environment of chloroplast acquisition by endosymbiosis and evolution of eukaryotic photosynthesis? Identification of cyanobacteria in the fossil record Paleontologists have to rely on information other than the genomic data and internal cellular organization to identify the biological affinities of early microfossils.
Ultrastructure The wall ultrastructure of modern cyanobacteria consists of a peptidoglycan layer of varying thickness in the periplasmic space between a cytoplasmic and an outer membrane, with generally an external S-layer [ 64 ]. Paleoecology and behavior Geochemical proxies may provide indirect evidence for oxygenation, at the planetary scale, such as the GOE, or at the scale of basins [ [73] , [74] , [75] , [76] , [77] ], and permit the reconstruction of the evolution of paleoredox conditions.
Molecular fossils Molecular fossils include complex organic molecules produced only by biology and, in some cases, are indicative of particular metabolisms or lineages [ 83 ].
Isotopic fractionation Carbon isotopes fractionation do not permit to discriminate oxygenic photosynthesis from other metabolisms that have overlapping range of fractionation, except for methanogenesis [ 98 , 99 ]. Intracellular biomineralization Passive biomineralization leads to precipitation of minerals on filaments, sheaths, or cells and enhance their preservation potential but is not specific of particular microorganisms [ , ].
The fossil record Microfossils interpreted as cyanobacteria have been reported in rocks as old as the early Archean, but their biogenicity and interpretation is highly debated. Table 1 Summary of microfossil morphological features, habitat, occurrences and their modern analogues. Presence of globose cells akinetes in or at the end of the filament. In aggregates, filaments are in a common mucilaginous matrix. If isolated, trichomes may be enveloped by an extracellular sheath thin and non-lamillated.
Benthic organism. Liulaobei Fm 0. The outer layers of colonies are pigmented. Branched or unbranched. Vesicles are usually with multilayered envelope. Apices may sometimes be tapered. Solitary or in mat-like mass. Cell length: 1, Trichome width: ; 25; 63 Shallow water marine environments, subtidal shelf environments, peritidal flat and pluvial lakes Bitter Springs Fm 0. Trichome surrounded by an uni- or multilayered smooth sheath.
The top of the stalk is open or is ended by preserved cells. Cells are dispersed or arranged in pairs, tetrads, octets or in colonies. Colonies sometimes arranged in pairs forming pseudobranched filament. Solitary or generally arranged in mass.
Unambiguous microfossils of cyanobacteria Although microfossils attributed to cyanobacteria are abundant during the Proterozoic, many of them are identified with some ambiguities.
Eoentophysalis The cyanobacteria fossil record starts around 1. Polybessurus Polybessurus is another Proterozoic microfossil unambiguously identified as a cyanobacterium [ ]. Eohyella The Limestone-Dolomite series of the ca. Probable and possible cyanobacteria microfossils Other microfossils are identified with less confidence but still considered as probable or possible cyanobacteria, depending on the authors.
Anhuithrix Pang et al. Archaeoellipsoides Nostocales and Stigonematales are modern cyanobacterial orders that, as mentioned above, have evolved specialized cells, the heterocytes [ ], and in some cases akinetes [ ].
Eomicrocystis Eomicrocystis is a microfossil genus described in by Golovenok and Belova [ ], and interpreted as a cyanobacteria. Gloeodiniopsis Gloeodiniopsis is also another possible fossil of a benthic chroococcacean cyanobacterium [ ]. Obruchevella Obruchevella is a microfossil that consists of an empty helically coiled tube Fig. Oscillatoriopsis Oscillatoriacean cyanobacteria are reported as the most represented group of cyanobacteria in the fossil record [ ]. Palaeolyngbya Palaeolyngbya is interpreted as a hormogonian oscillatoriocean cyanobacterium microfossil found first in the 0.
Polysphaeroides filiformis Polysphaeroides is a fossil genus described by Hermann [ ], which included several fossil species, until , when Hofmann and Jackson [ ] moved nearly all of the species of Polysphaeroides to the genus Chlorogloeaopsis , because of their similar morphology.
Siphonophycus Siphonophycus is one of the most common filamentous microfossils in the Proterozoic. Molecular dating The understanding of cyanobacterial phylum evolution has progressed significantly with the emergence of molecular biology techniques and new sequencing technologies.
Calibration, models, and datasets For molecular clock reconstructions, microfossils of cyanobacteria are needed as a source of calibration of the molecular phylogenies. Origin of cyanobacteria and oxygenic photosynthesis In most cyanobacterial phylogenetic analyses that are using a non-cyanobacterial outgroup to root the tree, the reference strain Gloeobacter violaceus PCC has a basal position [ 9 , [] , [] , [] ].
Diversification Several studies suggested that ancestral cyanobacteria first inhabited freshwater ecosystems [ 13 , 15 , 17 , , , ], but see e. Origin of chloroplast Chloroplasts form a monophyletic cluster within the Cyanobacteria phylum [ 12 ]. Conclusions Cyanobacterial fossil record starts unambiguously at 1. Acknowledgments We thank the editors W. Appendix A. Supplementary data The following is the Supplementary data to this article: Multimedia component 1: Click here to view.
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What Are the Two Prokaryotic Kingdoms? Role of Photosynthesis in Nature. Is Algae a Decomposer, a Scavenger or a Producer? Describe What a Photosystem Does for Photosynthesis. Role of Algae in the Ecosystem. How Does Photosynthesis Work in Plants? Percentage of Nitrogen in the Air. Types of Water Ecosystems.
How Does Photosynthesis Affect the Atmosphere of the
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