Diversity of Synechococcus and Prochlorococcus populations determined from DNA sequences of the N-regulatory gene ntcA

The cyanobacteria Synechococcus and Prochlorococcus are abundant primary producers in the nitrogen-poor waters of the Gulf of Aqaba, northern Red Sea. Expression of the nitrogen regulatory gene ntcA is a useful indicator for determining the N-status of cyanobacteria, and preliminary work with this gene suggests that it may also serve as a useful biodiversity marker. Here we investigated the genotypic diversity of ntcA among the full spectrum of cultured Synechococcus and Prochlorococcus lineages and assessed cyanobacterial genotypic composition in environmental samples from the Gulf of Aqaba. The high level of ntcA diversification established this gene as an excellent biodiversity marker capable of distinguishing between numerous clades within each genus with high resolution. An unexpected large diversity was observed among Synechococcus populations, including the detection of four novel clades for which culture representatives have yet to be isolated. In addition, extensive microdiversity within a number of Synechococcus clades was revealed. Temporal differences in the detection of the various Synechococcus clades suggest seasonal fluctuations in the genotypic make-up of Synechococcus populations. In contrast, virtually all Prochlorococcus sequences fell within a single high-light adapted clade that was detected year round. We suggest that the limited genotypic diversity among Prochlorococcus in combination with a limited capacity for acclimation to environmental changes resulting from its small genome size led to the dramatic rise and demise of Prochlorococcus populations over the yearly cycle in the Gulf of Aqaba.     

Analysis of the hli gene family in marine and freshwater cyanobacteria

Certain cyanobacteria thrive in natural habitats in which light intensities can reach 2000 micromol photon m(-2) s(-1) and nutrient levels are extremely low. Recently, a family of genes designated hli was demonstrated to be important for survival of cyanobacteria during exposure to high light. In this study we have identified members of the hli gene family in seven cyanobacterial genomes, including those of a marine cyanobacterium adapted to high-light growth in surface waters of the open ocean (Prochlorococcus sp. strain Med4), three marine cyanobacteria adapted to growth in moderate- or low-light (Prochlorococcus sp. strain MIT9313, Prochlorococcus marinus SS120, and Synechococcus WH8102), and three freshwater strains (the unicellular Synechocystis sp. strain PCC6803 and the filamentous species Nostoc punctiforme strain ATCC29133 and Anabaena sp. [Nostoc] strain PCC7120). The high-light-adapted Prochlorococcus Med4 has the smallest genome (1.7 Mb), yet it has more than twice as many hli genes as any of the other six cyanobacterial species, some of which appear to have arisen from recent duplication events. Based on cluster analysis, some groups of hli genes appear to be specific to either marine or freshwater cyanobacteria. This information is discussed with respect to the role of hli genes in the acclimation of cyanobacteria to high light, and the possible relationships among members of this diverse gene family.     

Glutamine synthetase from the marine cyanobacteria Prochlorococcus spp: characterization,phylogeny and response to nutrient limitation

The regulation of glutamine synthetase (EC 6.3.1.2) from Prochlorococcus was previously shown to exhibit unusual features: it is not upregulated by nitrogen starvation and it is not inactivated by darkness (El Alaoui et al. (2001) Appl Environ Microbiol 67: 2202-2207). These are probably caused by adaptations to oligotrophic environments, as confirmed in this work by the marked decrease in the enzymatic activity when cultures were subjected to iron or phosphorus starvation. In order to further understand the adaptive features of ammonium assimilation in this cyanobacterium, glutamine synthetase was purified from two Prochlorococcus strains: PCC 9511 (high-light adapted) and SS120 (low-light adapted). We obtained approximately 100-fold purified samples of glutamine synthetase electrophoretically homogeneous, with a yield of approximately 30%. The estimated molecular mass of the subunits was roughly the same for both strains: 48.3 kDa. The apparent Km constants for the biosynthetic activity were 0.30 mM for ammonium, 1.29 mM for glutamate and 1.35 mM for ATP; the optimum pH was 8.0. Optimal temperature was surprisingly high (55 degrees C). Phylogenetic analysis of glnA from three Prochlorococcus strains (MED4, MIT9313 and SS120) showed they group closely with marine Synechococcus isolates, in good agreement with other studies based on 16 S RNA sequences. All of our results suggest that the structure and kinetics of glutamine synthetase in Prochlorococcus have not been significantly modified during the evolution within the cyanobacterial radiation, in sharp contrast with its regulatory properties.     

Distribution patterns of marine planktonic cyanobacterial assemblages in transitional marine habitats using 16S rRNA phylogeny

The community composition of marine planktonic cyanobacteria in transitional marine habitats can influence its overall contribution to aquatic primary production. To understand distribution patterns of marine planktonic cyanobacterial assemblages, phylogenetic and statistical analyses were undertaken on planktonic cyanobacterial 16S rRNA gene sequences from four transitional marine habitats [Baltic Sea (BL), Monterey Bay (MB), South China Sea (SCS) and Sundarbans (SB)]. Out of 3255 sequences analyzed, only 546 sequences were found to be planktonic cyanobacteria and were considered in this study. Among these, 338 sequences representative of Sundarbans, the world's largest mangrove were generated based on Sanger and Illumina sequencing approaches. Based on 16S rRNA phylogeny, four major taxonomic orders of marine planktonic cyanobacteria were recovered in varying proportions with several novel 16S rRNA sequences in each of the four targeted sites. Members of the order Synechococcales were dominant in all the sites (?94% sequences) while the orders Chroococcales and Oscillatoriales were only detected in SB and SCS sites, respectively. In the phylogenetic tree, sequences representing the major marine picocyanobacterial genus Synechococcus showed overwhelming dominance in SB and they were found in three other sites. Prochlorococcus ‐like sequences were found in sizeable number in MB and SCS but were absent in SB and coastal BL. Synechococcus ‐like sequences were represented by three major marine clusters (5.1, 5.2, and 5.3). Three novel clades as part of Synechococcus cluster were detected only in SB and one novel clade in BL. The majority of OTUs were found to be exclusive to each site, whereas some were shared by two or more sites as revealed by beta‐diversity analysis.     

Culture isolation and culture-independent clone libraries reveal new marine Synechococcus ecotypes with distinctive light and N physiologies

Marine microbial communities often contain multiple closely related phylogenetic clades, but in many cases, it is still unclear what physiological traits differentiate these putative ecotypes. The numerically abundant marine cyanobacterium Synechococcus can be divided into at least 14 clades. In order to better understand ecotype differentiation in this genus, we assessed the diversity of a Synechococcus community from a well-mixed water column in the Sargasso Sea during March 2002, a time of year when this genus typically reaches its annual peak in abundance. Diversity was estimated from water sampled at three depths (approximately 5, 70, and 170 m) using both culture isolation and construction of cyanobacterial 16S-23S rRNA internal transcribed sequence clone libraries. Clonal isolates were obtained by enrichment with ammonium, nitrite, or nitrate as the sole N source, followed by pour plating. Each method sampled the in situ diversity differently. The combined methods revealed a total of seven Synechococcus phylotypes including two new putative ecotypes, labeled XV and XVI. Although most other isolates grow on nitrate, clade XV exhibited a reduced efficiency in nitrate utilization, and both clade XV and XVI are capable of chromatic adaptation, demonstrating that this trait is more widely distributed among Synechococcus strains than previously known. Thus, as in its sister genus Prochlorococcus, light and nitrogen utilization are important factors in ecotype differentiation in the marine Synechococcus lineage.     

Measurement of Prochlorococcus ecotypes using real-time polymerase chain reaction reveals different abundances of genotypes with similar light physiologies

Prochlorococcus is a marine cyanobacterium which is found at high abundances in world's tropical and subtropical oligotrophic oceans. The genus Prochlorococcus can be divided into two major groups based on light physiology. Both of these groups can be further subdivided into genetically distinct lineages, or ecotypes. Real-time polymerase chain reaction (PCR) assays based on sequence differences in the 16S-23S rDNA internal transcribed spacer or the 23S rDNA were developed to examine the distribution of each ecotype in the field. The real-time PCR assays enabled linear quantification of concentrations ranging from 10 to 4 x 10(5) cells ml(-1). These assays were applied to a stratified water column in the Sargasso Sea. The majority of Prochlorococcus cells above 110 m belonged to the one of the low chlorophyll b/a ratio (high-light adapted) ecotypes, while two types of high chlorophyll b/a ratio (low-light adapted) cells dominated below 110 m. The other three types were found at significantly lower numbers or not detected at all. Differences in the abundance of ecotypes within the major light physiology groupings suggest that other factors, such as nutrient utilization and differential mortality, are driving their relative distributions. Real-time PCR assays will enable further exploration of these factors and temporal and geographic variability in ecotype abundance.     

Distribution Pattern of Photosynthetic Picoplankton and Heterotrophic Bacteria in the Northern South China Sea

The environmental regulation of plcoplankton distribution in the northern South China Sea was examined In winter and summer of 2004. The average abundance of Synechococcus, Prochlorococcus, and heterotrophlc bacteria was lower In winter （30, 21, and 780×10^3 cells/cm^3, respectively） than In summer （53, 85, and 1 090×10^3 cells/cm^3, respectively）, but the seasonal pattern was opposite for plcoeukaryotlc phytoplankton （4 500 and 3 200 cells/cm^3 In winter and summer, respectively）. Synechococcus, picoeukaryotes, and bacteria were most abundant in the nutrient-rich coastal zone and continental shelf, but Prochlorococcus was most abundant In the continental slope and open ocean. The vertical distribution of each photosynthetic group and heterotrophlc bacteria changed between the two seasons. Synechococcus populations with apparently different phycoerythrobilin content occurred at many stations In the summer. In addition, two different populations of Prochlorococcus were found： （i） small, weakly fluorescing cells in the surface layer; and （ii） larger, strongly fluorescent cells In the deep layer. The distribution pattern of photosynthetic plcoplankton and heterotrophlc bacteria depends on environmental effects and their ecophyslologlcal differences. The distribution of Synechococcus appeared to be related to nutrient availability, whereas the distribution of Prochlorococcus appeared to be limited by temperature. Synechococcus was the only plcophytoplankton with a consistent strong relationship with bacteria.     

On-board flow cytometric observation of picoplankton community structure in the East China Sea during the fall of different years

On-board flow cytometric determinations of picoplankton abundance (i.e. Synechococcus spp., Prochlorococcus spp., picoeukaryotes and also heterotrophic bacteria) were obtained in the East China Sea in fall of 2000 and 2003. The average abundances of Synechococcus, Prochlorococcus, picoeukaryotes and heterotrophic bacteria were 10(5), 10(5), 10(4) and 10(6) cells ml(-1), respectively. Synechococcus, picoeukaryotes and heterotrophic bacteria were abundant at all the stations and presented higher concentration in the inner shelf where influences from the Changjiang effluent plumes and the coastal upwelling were evident, while Prochlorococcus was absent from the near-shore stations and became the dominant picophytoplankton population in offshore waters, where its abundance was comparable to that for heterotrophic bacteria. All picoplankton groups showed a reduction in cell number with depth, and a positive correlation with water temperature were observed, which reflected the importance of light and temperature on picoplankton growth. A negative relationship with salinity was found for heterotrophic bacteria along two sections across the East China Sea Shelf, and distribution of picoplankton was dominated by different water masses. The fixation could lead to loss in Prochlorococcus cell numbers within one month, and all the picoplankton numbers decreased dramatically after three months.     

Niche-partitioning of Prochlorococcus populations in a stratified water column in the eastern North Atlantic Ocean.

The in situ community structure of Prochlorococcus populations in the eastern North Atlantic Ocean was examined by analysis of Prochlorococcus 16S rDNA sequences with three independent approaches: cloning and sequencing, hybridization to specific oligonucleotide probes, and denaturing gradient gel electrophoresis (DGGE). The hybridization of high-light (HL) and low-light (LL) Prochlorococcus genotype-specific probes to two depth profiles of PCR-amplified 16S rDNA sequences revealed that in these two stratified water columns, an obvious niche-partitioning of Prochlorococcus genotypes occurred. In each water column a shift from the HL to the LL genotype was observed, a transition correlating with the depth of the surface mixed layer (SML). Only the HL genotype was found in the SML in each water column, whereas the LL genotype was distributed below the SML. The range of in situ irradiance to which each genotype was subjected within these distinct niches was consistent with growth irradiance studies of cultured HL- and LL-adapted Prochlorococcus strains. DGGE analysis and the sequencing of Prochlorococcus 16S rDNA clones were in full agreement with the genotype-specific oligonucleotide probe hybridization data. These observations of a partitioning of Prochlorococcus genotypes in a stratified water column provide a genetic basis for the dim and bright Prochlorococcus populations observed in flow cytometric signatures in several oceanic provinces.     

Light variability illuminates niche-partitioning among marine Picocyanobacteria

Prochlorococcus and Synechococcus picocyanobacteria are dominant contributors to marine primary production over large areas of the ocean. Phytoplankton cells are entrained in the water column and are thus often exposed to rapid changes in irradiance within the upper mixed layer of the ocean. An upward fluctuation in irradiance can result in photosystem II photoinactivation exceeding counteracting repair rates through protein turnover, thereby leading to net photoinhibition of primary productivity, and potentially cell death. Here we show that the effective cross-section for photosystem II photoinactivation is conserved across the picocyanobacteria, but that their photosystem II repair capacity and protein-specific photosystem II light capture are negatively correlated and vary widely across the strains. The differences in repair rate correspond to the light and nutrient conditions that characterize the site of origin of the Prochlorococcus and Synechococcus isolates, and determine the upward fluctuation in irradiance they can tolerate, indicating that photoinhibition due to transient high-light exposure influences their distribution in the ocean.     

Genome reduction by deletion of paralogs in the marine cyanobacterium Prochlorococcus

Several isolates of the marine cyanobacterial genus Prochlorococcus have smaller genome sizes than those of the closely related genus Synechococcus. In order to test whether loss of protein-coding genes has contributed to genome size reduction in Prochlorococcus, we reconstructed events of gene family evolution over a strongly supported phylogeny of 12 Prochlorococcus genomes and 9 Synechococcus genomes. Significantly, more events both of loss of paralogs within gene families and of loss of entire gene families occurred in Prochlorococcus than in Synechococcus. The number of nonancestral gene families in genomes of both genera was positively correlated with the extent of genomic islands (GIs), consistent with the hypothesis that horizontal gene transfer (HGT) is associated with GIs. However, even when only isolates with comparable extents of GIs were compared, significantly more events of gene family loss and of paralog loss were seen in Prochlorococcus than in Synechococcus, implying that HGT is not the primary reason for the genome size difference between the two genera.     

Distribution and Diversity of Microbial Eukaryotes in Bathypelagic Waters of the South China Sea

Little is known about the biodiversity of microbial eukaryotes in the South China Sea, especially in waters at bathyal depths. Here, we employed SSU rDNA gene sequencing to reveal the diversity and community structure across depth and distance gradients in the South China Sea. Vertically, the highest alpha diversity was found at 75‐m depth. The communities of microbial eukaryotes were clustered into shallow‐, middle‐, and deep‐water groups according to the depth from which they were collected, indicating a depth‐related diversity and distribution pattern. Rhizaria sequences dominated the microeukaryote community and occurred in all samples except those from less than 50‐m deep, being most abundant near the sea floor where they contributed ca. 64–97% and 40–74% of the total sequences and OTUs recovered, respectively. A large portion of rhizarian OTUs has neither a nearest named neighbor nor a nearest neighbor in the GenBank database which indicated the presence of new phylotypes in the South China Sea. Given their overwhelming abundance and richness, further phylogenetic analysis of rhizarians were performed and three new genetic clusters were revealed containing sequences retrieved from the deep waters of the South China Sea. Our results shed light on the diversity and community structure of microbial eukaryotes in this not yet fully explored area.     

Allochthonous inputs of riverine picocyanobacteria to coastal waters in the Arctic Ocean

The observed onset of climate change at high northern latitudes has highlighted the need to establish current baseline conditions in the Arctic Ocean, and has raised concern about the potential for the invasion and growth of biota that have warm temperature optima, such as cyanobacteria. In this study, we used 16S rRNA gene sequences as a molecular marker to evaluate the hypothesis that Arctic rivers provide a major inoculum of cyanobacteria into the coastal Arctic Ocean. Surface samples were collected along a transect extending from the Mackenzie River (Northwest Territories, Canada), across its estuary, to 200 km offshore at the edge of the perennial Arctic pack ice (Beaufort Sea). The highest picocyanobacteria concentrations occurred in the river, with concentrations an order of magnitude lower at offshore marine stations. The 16S rRNA gene clone libraries of five surface samples and five strains along this gradient showed that the cyanobacterial sequences were divided into eight operational taxonomic units (OTUs), six OTUs closely related to freshwater and brackish Synechococcus and two OTUs of filamentous cyanobacteria. No typically marine Synechococcus sequences and no Prochlorococcus sequences were recovered. These results are consistent with the hypothesis of an allochthonous origin of picocyanobacteria in the coastal Arctic Ocean, and imply survival but little net growth of picocyanobacteria under the present conditions in northern high-latitude seas.     

Cyanobacterial community structure as seen from RNA polymerase gene sequence analysis.

PCR was used to amplify DNA-dependent RNA polymerase gene sequences specifically from the cyanobacterial population in a seawater sample from the Sargasso Sea. Sequencing and analysis of the cloned fragments suggest that the population in the sample consisted of two distinct clusters of Prochlorococcus-like cyanobacteria and four clusters of Synechococcus-like cyanobacteria. The diversity within these clusters was significantly different, however. Clones within each Synechococcus-like cluster were 99 to 100% identical, while each Prochlorococcus-like cluster was only 91% identical at the nucleotide level. One Prochlorococcus-like cluster was significantly more closely related to a Mediterranean Sea (surface) Prochlorococcus isolate than to the other cluster, showing the highly divergent nature of this group even in one sample. The approach described here can be used as a general method for examining cyanobacterial diversity, while an oligotrophic ocean ecosystem such as the Sargasso Sea may be an ideal model for examining diversity in relation to environmental parameters.     

PRESENCE OF PHYCOERYTHRIN IN TWO STRAINS OF PROCHLOROCOCCUS (CYANOBACTERIA) ISOLATED FROM THE SUBTROPICAL NORTH PACIFIC OCEAN

Prochlorococcus is a ubiquitous marine oxyphotobacterium characterized by the presence of DV-chl a and b . In addition, the type strain Prochlorococcus marinus Chisholm et al. CCMP 1375 (or SS120), an isolate from the Sargasso Sea, contains low levels of an unusual phycoerythrin. Until now, it has been unclear if phycoerythrin occurs randomly within this systematic group and if the molecular characteristics of this phycoerythrin are restricted to this single strain. Here, we show that two additional Prochlorococcus strains from the Pacific Ocean also contain similar low levels of phycoerythrin. DNA sequence and phylogenetic analyses demonstrated that this phycoerythrin is very similar to the phycoerythrin of P. marinus SS120 and differs from the classic cyanobacterial phycoerythrins. In contrast, a third isolate from the Arabian Sea lacks phycoerythrin. Based on the DV-chl b:a ratio and 16S rRNA sequence data, we classify the two Pacific phycoerythrin-containing isolates as low-light-adapted strains and the Arabian Sea isolate as a high-light-adapted strain. Thus, we provide further evidence to link the physiology of an individual genotype and the presence or absence of functional phycoerythrin genes within the genus Prochlorococcus .     

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.     

从营养扰动实验看原绿球藻在近海分布的制约因素

地球上细胞最小、丰度最大的放氧光合自养原核生物原绿球藻 (Prochlorococcus)发现于热带大洋 ,并被证实可在某些近海甚至近岸水域大量分布。但除温度之外 ,原绿球藻自然分布的控制因子尚不明了。从近海和大洋生态条件的主要差别考虑 ,在南海进行了主要营养盐———氮、磷和微量元素———铁、钴扰动的现场培养实验 ,并应用流式细胞技术监测原绿球藻及聚球藻 (Synechococcus)、超微型真核浮游植物 (pico_eukaryotes)的细胞丰度和单细胞色素含量的响应以及细菌的影响。结果表明 ,磷和钴的添加有利于原绿球藻 ,而氮和铁的添加更有利于聚球藻和超微型真核浮游植物。同时 ,由环境条件引起的生物响应又间接地导致超微型生物之间的相互作用。因而 ,原绿球藻在近海的分布 ,可能受到营养盐组成等环境因子以及生物之间的相互作用等多方面的限制和影响     

Resolution of Prochlorococcus and Synechococcus ecotypes by using 16S-23S ribosomal DNA internal transcribed spacer sequences

Cultured isolates of the marine cyanobacteria Prochlorococcus and Synechococcus vary widely in their pigment compositions and growth responses to light and nutrients, yet show greater than 96% identity in their 16S ribosomal DNA (rDNA) sequences. In order to better define the genetic variation that accompanies their physiological diversity, sequences for the 16S-23S rDNA internal transcribed spacer (ITS) region were determined in 32 Prochlorococcus isolates and 25 Synechococcus isolates from around the globe. Each strain examined yielded one ITS sequence that contained two tRNA genes. Dramatic variations in the length and G+C content of the spacer were observed among the strains, particularly among Prochlorococcus strains. Secondary-structure models of the ITS were predicted in order to facilitate alignment of the sequences for phylogenetic analyses. The previously observed division of Prochlorococcus into two ecotypes (called high and low-B/A after their differences in chlorophyll content) were supported, as was the subdivision of the high-B/A ecotype into four genetically distinct clades. ITS-based phylogenies partitioned marine cluster A Synechococcus into six clades, three of which can be associated with a particular phenotype (motility, chromatic adaptation, and lack of phycourobilin). The pattern of sequence divergence within and between clades is suggestive of a mode of evolution driven by adaptive sweeps and implies that each clade represents an ecologically distinct population. Furthermore, many of the clades consist of strains isolated from disparate regions of the world's oceans, implying that they are geographically widely distributed. These results provide further evidence that natural populations of Prochlorococcus and Synechococcus consist of multiple coexisting ecotypes, genetically closely related but physiologically distinct, which may vary in relative abundance with changing environmental conditions.     

Synechococcus diversity in the California current as seen by RNA polymerase (rpoC1) gene sequences of isolated strains.

Because they are ubiquitous in a range of aquatic environments and culture methods are relatively advanced, cyanobacteria may be useful models for understanding the extent of evolutionary adaptation of prokaryotes in general to environmental gradients. The roles of environmental variables such as light and nutrients in influencing cyanobacterial genetic diversity are still poorly characterized, however. In this study, a total of 15 Synechococcus strains were isolated from the oligotrophic edge of the California Current from two depths (5 and 95 m) with large differences in light intensity, light quality, and nutrient concentrations. RNA polymerase gene (rpoC1) fragment sequences of the strains revealed two major genetic lineages, distinct from other marine or freshwater cyanobacterial isolates or groups seen in shotgun-cloned sequences from the oligotrophic Atlantic Ocean. The California Current low-phycourobilin (CCLPUB) group represented by six isolates in a single lineage was less diverse than the California Current high-phycourobilin (CCHPUB) group with nine isolates in three relatively divergent lineages. The former was found to be the closest known genetic group to Prochlorococcus spp., a chlorophyll b-containing cyanobacterial group. Having an isolate from this group will be valuable for looking at the molecular changes necessary for the transition from the use of phycobiliproteins to chlorophyll b as light-harvesting pigments. Both of the CCHPUB and CCLPUB groups included strains obtained from surface (5 m) and deep (95 m) samples. Thus, contrary to expectations, there was no clear correlation between sampling depth and isolation of genetic groups, despite the large environmental gradients present. To our knowledge, this is the first demonstration with isolates that genetically divergent Synechococcus groups coexist in the same seawater sample.     

Dependence of the cyanobacterium Prochlorococcus on hydrogen peroxide scavenging microbes for growth at the ocean's surface

The phytoplankton community in the oligotrophic open ocean is numerically dominated by the cyanobacterium Prochlorococcus, accounting for approximately half of all photosynthesis. In the illuminated euphotic zone where Prochlorococcus grows, reactive oxygen species are continuously generated via photochemical reactions with dissolved organic matter. However, Prochlorococcus genomes lack catalase and additional protective mechanisms common in other aerobes, and this genus is highly susceptible to oxidative damage from hydrogen peroxide (HOOH). In this study we showed that the extant microbial community plays a vital, previously unrecognized role in cross-protecting Prochlorococcus from oxidative damage in the surface mixed layer of the oligotrophic ocean. Microbes are the primary HOOH sink in marine systems, and in the absence of the microbial community, surface waters in the Atlantic and Pacific Ocean accumulated HOOH to concentrations that were lethal for Prochlorococcus cultures. In laboratory experiments with the marine heterotroph Alteromonas sp., serving as a proxy for the natural community of HOOH-degrading microbes, bacterial depletion of HOOH from the extracellular milieu prevented oxidative damage to the cell envelope and photosystems of co-cultured Prochlorococcus, and facilitated the growth of Prochlorococcus at ecologically-relevant cell concentrations. Curiously, the more recently evolved lineages of Prochlorococcus that exploit the surface mixed layer niche were also the most sensitive to HOOH. The genomic streamlining of these evolved lineages during adaptation to the high-light exposed upper euphotic zone thus appears to be coincident with an acquired dependency on the extant HOOH-consuming community. These results underscore the importance of (indirect) biotic interactions in establishing niche boundaries, and highlight the impacts that community-level responses to stress may have in the ecological and evolutionary outcomes for co-existing species.