Co-occurring Synechococcus ecotypes occupy four major oceanic regimes defined by temperature,macronutrients and iron

Marine picocyanobacteria, comprised of the genera Synechococcus and Prochlorococcus, are the most abundant and widespread primary producers in the ocean. More than 20 genetically distinct clades of marine Synechococcus have been identified, but their physiology and biogeography are not as thoroughly characterized as those of Prochlorococcus. Using clade-specific qPCR primers, we measured the abundance of 10 Synechococcus clades at 92 locations in surface waters of the Atlantic and Pacific Oceans. We found that Synechococcus partition the ocean into four distinct regimes distinguished by temperature, macronutrients and iron availability. Clades I and IV were prevalent in colder, mesotrophic waters; clades II, III and X dominated in the warm, oligotrophic open ocean; clades CRD1 and CRD2 were restricted to sites with low iron availability; and clades XV and XVI were only found in transitional waters at the edges of the other biomes. Overall, clade II was the most ubiquitous clade investigated and was the dominant clade in the largest biome, the oligotrophic open ocean. Co-occurring clades that occupy the same regime belong to distinct evolutionary lineages within Synechococcus, indicating that multiple ecotypes have evolved independently to occupy similar niches and represent examples of parallel evolution. We speculate that parallel evolution of ecotypes may be a common feature of diverse marine microbial communities that contributes to functional redundancy and the potential for resiliency.     

Comparative membrane proteomics reveal contrasting adaptation strategies for coastal and oceanic marine Synechococcus cyanobacteria

Marine cyanobacteria genus Synechococcus are among the most abundant and widespread primary producers in the open ocean. Synechococcus strains belonging to different clades have adapted distinct strategies for growth and survival across a range of marine conditions. Clades I and IV are prevalent in colder, mesotrophic, coastal waters, while clades II and III prefer warm, oligotrophic open oceans. To gain insight into the cellular resources these unicellular organisms invest in adaptation strategies we performed shotgun membrane proteomics of four Synechococcus spp. strains namely CC9311 (clade I), CC9605 (clade II), WH8102 (clade III) and CC9902 (clade IV). Comparative membrane proteomes analysis demonstrated that CC9902 and WH8102 showed high resource allocation for phosphate uptake, accounting for 44% and 38% of overall transporter protein expression of the species. WH8102 showed high expression of the iron uptake ATP-binding cassette binding protein FutA, suggesting that a high binding affinity for iron is possibly a key adaptation strategy for some strains in oligotrophic ocean environments. One protein annotated as a phosphatase 2c (Sync_2505 and Syncc9902_0387) was highly expressed in the coastal mesotrophic strains CC9311 and CC9902, constituting 14%–16% of total membrane protein, indicating a vital, but undefined function, for strains living in temperate mesotrophic environments.     

Global phylogeography of marine Synechococcus and Prochlorococcus reveals a distinct partitioning of lineages among oceanic biomes

Marine cyanobacteria of the genera Prochlorococcus and Synechococcus are important contributors to global primary production occupying a key position at the base of marine food webs. The genetically diverse nature of each genus is likely an important reason for their successful colonization of vast tracts of the world's oceans, a feature that has led to detailed analysis of the distribution of these genetic lineages at the local and ocean basin scale. Here, we extend these analyses to the global dimension, using new data from cruises in the Pacific, Indian and Arctic Oceans in combination with data from previous studies in the Atlantic Ocean, Arabian Sea, Red Sea and a circumnavigation of the southern hemisphere to form a data set which comprises most of the world's major ocean systems. We show that the distribution patterns of Prochlorococcus and Synechococcus lineages are remarkably similar in different ocean systems with comparable environmental conditions, but producing a strikingly different 'signature' in the four major ocean domains or biomes (the Polar Domain, Coastal Boundary Domain, Trade Winds Domain and Westerly Winds Domain). This clearly reiterates the idea of spatial partitioning of individual cyanobacterial lineages, but at the global scale.     

Biochemical bases of type IV chromatic adaptation in marine Synechococcus spp

Chromatic adaptation (CA) in cyanobacteria has provided a model system for the study of the environmental control of photophysiology for several decades. All forms of CA that have been examined so far (types II and III) involve changes in the relative contents of phycoerythrin (PE) and/or phycocyanin when cells are shifted from red to green light and vice versa. However, the chromophore compositions of these polypeptides are not altered. Some marine Synechococcus species strains, which possess two PE forms (PEI and PEII), carry out another type of CA (type IV), occurring during shifts from blue to green or white light. Two chromatically adapting strains of marine Synechococcus recently isolated from the Gulf of Mexico were utilized to elucidate the mechanism of type IV CA. During this process, no change in the relative contents of PEI and PEII was observed. Instead, the ratio of the two chromophores bound to PEII, phycourobilin and phycoerythrobilin, is high under blue light and low under white light. Mass spectroscopy analyses of isolated PEII alpha- and beta-subunits show that there is a single PEII protein type under all light climates. The CA process seems to specifically affect the chromophorylation of the PEII (and possibly PEI) alpha chain. We propose a likely process for type IV CA, which involves the enzymatic activity of one or several phycobilin lyases and/or lyase-isomerases differentially controlled by the ambient light quality. Phylogenetic analyses based on the 16S rRNA gene confirm that type IV CA is not limited to a single clade of marine Synechococcus.     

Proteomic comparison between two marine snail ecotypes reveals details about the biochemistry of adaptation

The proteomic changes occurring during speciation are fundamental to understand this process, though they have been rarely addressed until present. Therefore, we compared the proteome of two ecotypes (RB and SU) of the marine snail Littorina saxatilis, a case of sympatric incomplete speciation, originated as a byproduct of adaptation to distinct habitats. Thus, the RB ecotype is able to resist stresses of desiccation and temperature on the upper shore, whereas the SU ecotype defies strong physical disturbances due to wave action. Qualitative analyses of 2-DE gels demonstrated 21 proteins differentially expressed (1.4% of the proteome, 1.2% after considering type-I errors), while quantitative changes accounted for differences in 22 spots (16% of the proteome, 11% after considering type-I errors). These results suggest that adaptative phenotypic plasticity, natural selection, or both maintain these ecotypes in sympatry. Among the proteins identified by MS, we found that fructose-bisphosphate aldolase and arginine kinase were up-regulated in the SU ecotype, suggesting an enhancement of the level of energy available as ATP, in order to withstand its wave-exposed habitat.     

Genomic evidence for distinct carbon substrate preferences and ecological niches of Bathyarchaeota in estuarine sediments

Investigations of the biogeochemical roles of benthic Archaea in marine sediments are hampered by the scarcity of cultured representatives. In order to determine their metabolic capacity, we reconstructed the genomic content of four widespread uncultured benthic Archaea recovered from estuary sediments at 48% to 95% completeness. Four genomic bins were found to belong to different subgroups of the former Miscellaneous Crenarcheota Group (MCG) now called Bathyarchaeota: MCG‐6, MCG‐1, MCG‐7/17 and MCG‐15. Metabolic predictions based on gene content of the different genome bins indicate that subgroup 6 has the ability to hydrolyse extracellular plant‐derived carbohydrates, and that all four subgroups can degrade detrital proteins. Genes encoding enzymes involved in acetate production as well as in the reductive acetyl–CoA pathway were detected in all four genomes inferring that these Archaea are organo‐heterotrophic and autotrophic acetogens. Genes involved in nitrite reduction were detected in all Bathyarchaeota subgroups and indicate a potential for dissimilatory nitrite reduction to ammonium. Comparing the genome content of the different Bathyarchaeota subgroups indicated preferences for distinct types of carbohydrate substrates and implicitly, for different niches within the sedimentary environment.     

The role of phenotypic plasticity on the proteome differences between two sympatric marine snail ecotypes adapted to distinct micro-habitats

Background  

The role of phenotypic plasticity is increasingly being recognized in the field of evolutionary studies. In this paper we look at the role of genetic determination versus plastic response by comparing the protein expression profiles between two sympatric ecotypes adapted to different shore levels and habitats using two-dimensional protein maps.     

Genomic island genes in a coastal marine Synechococcus strain confer enhanced tolerance to copper and oxidative stress

Highly variable regions called genomic islands are found in the genomes of marine picocyanobacteria, and have been predicted to be involved in niche adaptation and the ecological success of these microbes. These picocyanobacteria are typically highly sensitive to copper stress and thus, increased copper tolerance could confer a selective advantage under some conditions seen in the marine environment. Through targeted gene inactivation of genomic island genes that were known to be upregulated in response to copper stress in Synechococcus sp. strain CC9311, we found two genes (sync_1495 and sync_1217) conferred tolerance to both methyl viologen and copper stress in culture. The prevalence of one gene, sync_1495, was then investigated in natural samples, and had a predictable temporal variability in abundance at a coastal monitoring site with higher abundance in winter months. Together, this shows that genomic island genes can confer an adaptive advantage to specific stresses in marine Synechococcus, and may help structure their population diversity.     

Genomic and structural analysis of Syn9, a cyanophage infecting marine Prochlorococcus and Synechococcus

Cyanobacteriophage Syn9 is a large, contractile-tailed bacteriophage infecting the widespread, numerically dominant marine cyanobacteria of the genera Prochlorococcus and Synechococcus . Its 177 300 bp genome sequence encodes 226 putative proteins and six tRNAs. Experimental and computational analyses identified genes likely involved in virion formation, nucleotide synthesis, and DNA replication and repair. Syn9 shows significant mosaicism when compared with related cyanophages S-PM2, P-SSM2 and P-SSM4, although shared genes show strong purifying selection and evidence for large population sizes relative to other phages. Related to coliphage T4 – which shares 19% of Syn9's genes – Syn9 shows evidence for different patterns of DNA replication and uses homologous proteins to assemble capsids with a different overall structure that shares topology with phage SPO1 and herpes virus. Noteworthy bacteria-related sequences in the Syn9 genome potentially encode subunits of the photosynthetic reaction centre, electron transport proteins, three pentose pathway enzymes and two tryptophan halogenases. These genes suggest that Syn9 is well adapted to the physiology of its photosynthetic hosts and may affect the evolution of these sequences within marine cyanobacteria.     

The marine picoplankter Synechococcus sp. WH 7803 exhibits an adaptive response to restricted iron availability

Abstract: Laboratory cultures of marine Synechococcus sp. WH 7803 were grown under conditions of restricted iron availability. The culture medium was adjusted to restrict iron availability: (i) by adding the iron chelator EDDA; (ii) by omitting iron; and (iii) by omitting both iron and EDTA. An adaptive response was observed to these iron-restricted conditions, including a decrease in cellular phycoerythrin and synthesis of a 36 kDa polypeptide in [³⁵S]methionine radiolabelled whole cell lysates separated by SDS-PAGE. The polypeptide was synthesized within 48 h of transferring exponential phase cells to the iron-restricted medium. The protein was localized to the cell membranes and not the cytoplasmic fraction.     

Silicon deficiency and the adaptation of tropical rice ecotypes

Although silicon (Si) is found at much higher concentrations in healthy rice crops than N, P or K, it has received far less study, particularly for upland rice. There are few reports on the existence, causes, and effects of varying Si supplies in different environments. Chemical analyses of soil, water and plant tissue samples from experiments grown on a typical weathered, acidic upland soil in Colombia found concentrations of Si which were 80-90% lower than those in a typical lowland environment. These results corroborate published findings from West Africa and Hawaii, and lend support to a conclusion that acid-soil upland rice environments in the tropics tend to be deficient in Si, increasing disease damage, among other effects. Critical values for diagnosis of Si deficiency in soils, water and rice husk tissue are suggested. These are reasonably consistent with, but extend the application of previously published values derived from lowland rice studies to upland environments, and use simpler sampling and analysis methods. A strong correlation was found (r = -0.91) between high husk Si concentration and low husk discoloration disease damage, among diverse rice genotypes grown in the uplands. These genotypic differences were mainly explained by their ecotypic affinities: those belonging to the tropical japonica ecotype exhibited 93% higher husk Si concentrations than indica ecotypes (ecotypic means of 23 vs. 12 mg kg^-1 ). This is consistent with a hypothesis that the tropical japonicas may have adapted to Si deficiency in their native upland environment by evolving mechanisms to attain relatively higher tissue Si concentrations than indicas, which are believed to have evolved in the lowlands, where the Si supply is generally ample. Increased understanding of Si-mediated disease resistance in different rice environments and ecotypes could help breeders combine the high yield potential of indica types with the more durable disease resistance of the japonicas, and could contribute to the development of integrated disease management strategies.     

Iron stress genes in marine Synechococcus and the development of a flow cytometric iron stress assay

Marine Synechococcus are frequently found in environments where iron (Fe) is a limiting nutrient. To understand their capacity to respond to Fe stress, we screened picoplankton genomes and the Global Ocean Survey metagenome for known Fe stress genes. Many open ocean strains of Synechococcus lack most known genes for Fe stress, while coastal and upwelling strains contain many, suggesting that maintaining multiple Fe limitation compensation strategies is not a selective advantage in the open ocean. All genomes contained iron deficiency-induced protein A (IdiA) and its complementary Fe³⁺ transport proteins. The ubiquity of IdiA was exploited to develop an in situ Fe stress bioassay based on immunolabelling and flow cytometry. As a test of field applicability, we used the assay on natural Synechococcus populations from one station in the Costa Rica Upwelling Dome where total Fe ranged from <0.08 to 0.14 nM in the upper water column. The bioassay found Fe stress in 5–54% of the population. Based on our findings, we believe that when reactive strains are present this assay can reveal environmental and clade-specific differences in the response of Synechococcus to Fe stress.     

A genetic manipulation system for oceanic cyanobacteria of the genus Synechococcus.

Unicellular cyanobacteria of the genus Synechococcus are among the most abundant members of the picoplankton in the open ocean, and their contribution to primary production is considerable. While several isolates have been used for physiological, biochemical, and molecular studies of their unique adaptations to the marine environment, it has become necessary to develop molecular genetic methods for one or more model open-ocean cyanobacteria in order for studies of these organisms and their unique properties to progress. A number of molecular tools for the genetic manipulation of Synechococcus sp. strains WH7803, WH8102, and WH8103 have been developed. These include a plating technique for obtaining isolated colonies at high efficiencies and a conjugation method for introducing both a replicative vector and a suicide vector. In addition, a method for the generation of random, tagged chromosomal insertions (N. Dolganov and A. R. Grossman, J. Bacteriol. 175:7644-7651, 1993; N. F. Tsinoremas, A. K. Kutach, C. A. Strayer, and S. S. Golden, J. Bacteriol. 176:6764-6768, 1994) has been applied to these organisms.     

The importance of phenotypic plasticity and local adaptation in driving intraspecific variability in thermal niches of marine macrophytes

Climate change is driving the redistribution of species at a global scale and documenting and predicting species' responses to warming is a principal focus of contemporary ecology. When interpreting and predicting their responses to warming, species are generally treated as single homogenous physiological units. However, local adaptation and phenotypic plasticity can result in intraspecific differences in thermal niche. Therefore, population loss may also not only occur from trailing edges. In species with low dispersal capacity this will have profound impacts for the species as a whole, as local population loss will not be offset by immigration of warm tolerant individuals. Recent evidence from terrestrial forests has shown that incorporation of intraspecific variation in thermal niche is vital to accurately predicting species responses to warming. However, marine macrophytes (i.e. seagrasses and seaweeds) that form some of the world's most productive and diverse ecosystems have not been examined in the same context. We conducted a literature review to determine how common intraspecific variation in thermal physiology is in marine macrophytes. We find that 90% of studies identified (n = 42) found clear differences in thermal niche between geographically separated populations. Therefore, non‐trailing edge populations may also be vulnerable to future warming trends and given their limited dispersal capacity, such population loss may not be offset by immigration. We also explore how next generation sequencing (NGS) is allowing unprecedented mechanistic insight into plasticity and adaptation. We conclude that in the ‘genomic era’ it may be possible to link understanding of plasticity and adaptation at the genetic level through to changes in populations providing novel insights on the redistribution of populations under future climate change.     

Genomic divergence between the migratory and stationary ecotypes of Atlantic cod

Atlantic cod displays a range of phenotypic and genotypic variations, which includes the differentiation into coastal stationary and offshore migratory types of cod that co‐occur in several parts of its distribution range and are often sympatric on the spawning grounds. Differentiation of these ecotypes may involve both historical separation and adaptation to ecologically distinct environments, the genetic basis of which is now beginning to be unravelled. Genomic analyses based on recent sequencing advances are able to document genomic divergence in more detail and may facilitate the exploration of causes and consequences of genome‐wide patterns. We examined genomic divergence between the stationary and migratory types of cod in the Northeast Atlantic, using next‐generation sequencing of pooled DNA from each of two population samples. Sequence data was mapped to the published cod genome sequence, arranged in more than 6000 scaffolds (611 Mb). We identified 25 divergent scaffolds (26 Mb) with a higher than average gene density, against a backdrop of overall moderate genomic differentiation. Previous findings of localized genomic divergence in three linkage groups were confirmed, including a large (15 Mb) genomic region, which seems to be uniquely involved in the divergence of migratory and stationary cod. The results of the pooled sequencing approach support and extend recent findings based on single‐nucleotide polymorphism markers and suggest a high degree of reproductive isolation between stationary and migratory cod in the North‐east Atlantic.     

Effects of iron on the growth and minimal fluorescence yield of three marine Synechococcus strains (Cyanophyceae)

Two coastal Synechococcus stains PCC 7002 and CC9311 and one oceanic strain WH8102 were cultured with 4–1000 nM Fe in Aquil medium. Compared with those under iron‐replete conditions, their growth rates were significantly decreased by 59% for WH8102 at 15 nM Fe, by 37% for CC9311 at 15 nM Fe and by 57% for PCC 7002 at 4 nM Fe. Among these three strains, PCC 7002 was the most tolerant to iron limitation while WH8102 was the most sensitive to iron limitation. For each strain under the same iron concentration, the growth rates calculated from the minimal fluorescence yield and cell concentration showed no significant difference. The linear correlation was established between the minimal fluorescence yield and cell concentration although the minimal fluorescence yield per cell varied depending on the strains and iron levels. Under iron‐replete conditions, the minimal fluorescence yield per cell was 100‐fold higher for the phycoerythrin‐lacking strain PCC 7002 than two phycoerythrin‐containing strains WH8102 and CC9311. Under iron‐deplete conditions, it was increased respectively by 128% and 7% for WH8102 and CC9311 but was decreased by 30% for PCC 7002. Furthermore, the minimal fluorescence yield per cell for PCC 7002 and CC9311 showed little difference throughout the light and dark diel cycle. However, it was significantly higher for WH8102 in the daytime than in the dark.     

The role of respiration during adaptation of the freshwater cyanobacterium Synechococcus 6311 to salinity

Growth of the freshwater cyanobacterium Synechococcus 6311 under saline conditions stimulated respiration tenfold during the first 24 h, while growth and photosynthesis were inhibited. The elevated respiration rate was seen under both light and dark conditions, was uncoupler and cyanide sensitive, and did not decrease upon salt removal. Membrane preparations from salt-grown cells exhibited a tenfold increase in cytochrome oxidase activity, while electron transfer rates from NADPH to cytochrome c only increased threefold. Cytochrome oxidase activities were correlated with levels of EPR detectable Cu2+ in the salt and control membranes. Sodium-driven proton (antiproter) gradients in salt-grown cells were sensitive to cyanide but not dicyclohexylcarbodiimide, indicating the direct role of respiratory electron transport in maintaining low intracellular sodium levels.     

Genomic imprinting and the units of adaptation

Two guiding principles identify which biological entities are able to evolve adaptations. Williams'' principle holds that, in order for an entity to evolve adaptations, there must be selection between such entities. Maynard Smith''s principle holds that, in order for an entity to evolve adaptations, selection within such entities must be absent or negligible. However, although the kinship theory of genomic imprinting suggests that parent-of-origin-specific gene expression evolves as a consequence of natural selection acting between—rather than within—individuals, it evades adaptive interpretation at the individual level and is instead viewed as an outcome of an intragenomic conflict of interest between an individual''s genes. Here, I formalize the idea that natural selection drives intragenomic conflicts of interest between genes originating from different parents. Specifically, I establish mathematical links between the dynamics of natural selection and the idea of the gene as an intentional, inclusive-fitness-maximizing agent, and I clarify the role that information about parent of origin plays in mediating conflicts of interest between genes residing in the same genome. These results highlight that the suppression of divisive information may be as important as the suppression of lower levels of selection in maintaining the integrity of units of adaptation.