Dual thermal ecotypes coexist within a nearly genetically identical population of the unicellular marine cyanobacterium Synechococcus.

The extent and ecological significance of intraspecific functional diversity within marine microbial populations is still poorly understood, and it remains unclear if such strain-level microdiversity will affect fitness and persistence in a rapidly changing ocean environment. In this study, we cultured 11 sympatric strains of the ubiquitous marine picocyanobacterium Synechococcus isolated from a Narragansett Bay (RI) phytoplankton community thermal selection experiment. Thermal performance curves revealed selection at cool and warm temperatures had subdivided the initial population into thermotypes with pronounced differences in maximum growth temperatures. Curiously, the genomes of all 11 isolates were almost identical (average nucleotide identities of >99.99%, with >99% of the genome aligning) and no differences in gene content or single nucleotide variants were associated with either cool or warm temperature phenotypes. Despite a very high level of genomic similarity, sequenced epigenomes for two strains showed differences in methylation on genes associated with photosynthesis. These corresponded to measured differences in photophysiology, suggesting a potential pathway for future mechanistic research into thermal microdiversity. Our study demonstrates that present-day marine microbial populations can harbor cryptic but environmentally relevant thermotypes which may increase their resilience to future rising temperatures.

Marine Synechococcus isolates representing globally abundant genomic lineages demonstrate a unique evolutionary path of genome reduction without a decrease in GC content.

Synechococcus, a genus of unicellular cyanobacteria found throughout the global surface ocean, is a large driver of Earth's carbon cycle. Developing a better understanding of its diversity and distributions is an ongoing effort in biological oceanography. Here, we introduce 12 new draft genomes of marine Synechococcus isolates spanning five clades and utilize ~100 environmental metagenomes largely sourced from the TARA Oceans project to assess the global distributions of the genomic lineages they and other reference genomes represent. We show that five newly provided clade-II isolates are by far the most representative of the recovered in situ populations (most 'abundant') and have biogeographic distributions distinct from previously available clade-II references. Additionally, these isolates form a subclade possessing the smallest genomes yet identified of the genus (2.14 ± 0.05Mbps; mean ± 1SD) while concurrently hosting some of the highest GC contents (60.67 ± 0.16%). This is in direct opposition to the pattern in Synechococcus's nearest relative, Prochlorococcus - wherein decreasing genome size has coincided with a strong decrease in GC content - suggesting this new subclade of Synechococcus appears to have convergently undergone genomic reduction relative to the rest of the genus, but along a fundamentally different evolutionary trajectory.

Genome Sequence of Synechococcus sp. Strain LA31, Isolated from a Temperate Estuary.

Cluster 5 Synechococcus species are widely acknowledged for their broad distribution and biogeochemical importance. In particular, subcluster 5.2 strains inhabit freshwater, estuarine, and marine environments but are understudied, compared to other subclusters. Here, we present the genome for Synechococcus sp. strain LA31, a strain that was recently isolated from Narragansett Bay, Rhode Island, USA.

Two co-dominant nitrogen-fixing cyanobacteria demonstrate distinct acclimation and adaptation responses to cope with ocean warming.

The globally dominant N2 -fixing cyanobacteria Trichodesmium and Crocosphaera provide vital nitrogen supplies to subtropical and tropical oceans, but little is known about how they will be affected by long-term ocean warming. We tested their thermal responses using experimental evolution methods during 2 years of selection at optimal (28°C), supra-optimal (32°C) and suboptimal (22°C) temperatures. After several hundred generations under thermal selection, changes in growth parameters, as well as N and C fixation rates, suggested that Trichodesmium did not adapt to the three selection temperature regimes during the 2-year evolution experiment, but could instead rapidly and reversibly acclimate to temperature shifts from 20°C to 34°C. In contrast, over the same timeframe apparent thermal adaptation was observed in Crocosphaera, as evidenced by irreversible phenotypic changes as well as whole-genome sequencing and variant analysis. Especially under stressful warming conditions (34°C), 32°C-selected Crocosphaera cells had an advantage in survival and nitrogen fixation over cell lines selected at 22°C and 28°C. The distinct strategies of phenotypic plasticity versus irreversible adaptation in these two sympatric diazotrophs are both viable ways to maintain fitness despite long-term temperature changes, and so could help to stabilize key ocean nitrogen cycle functions under future warming scenarios.

Transient exposure to novel high temperatures reshapes coastal phytoplankton communities.

Average sea surface temperatures are expected to rise 4° this century, and marine phytoplankton and bacterial community composition, biogeochemical rates, and trophic interactions are all expected to change in a future warmer ocean. Thermal experiments typically use constant temperatures; however, weather and hydrography cause marine temperatures to fluctuate on diel cycles and over multiple days. We incubated natural communities of phytoplankton collected from California coastal waters during spring, summer, and fall under present-day and future mean temperatures, using thermal treatments that were either constant or fluctuated on a 48 h cycle. As assayed by marker-gene sequencing, the emergent microbial communities were consistent within each season, except when culture temperatures exceeded the highest temperature recorded in a 10-year local thermal dataset. When temperature treatments exceeded the 10-year maximum the phytoplankton community shifted, becoming dominated by diatom amplicon sequence variants (ASVs) not seen at lower temperatures. When mean temperatures were above the 10-year maximum, constant and fluctuating regimes each selected for different ASVs. These findings suggest coastal microbial communities are largely adapted to the current range of temperatures they experience. They also suggest a general hypothesis whereby multiyear upper temperature limits may represent thresholds, beyond which large community restructurings may occur. Now inevitable future temperature increases that exceed these environmental thresholds, even temporarily, may fundamentally reshape marine microbial communities and therefore the biogeochemical cycles that they mediate.

Distinct Responses of the Nitrogen-Fixing Marine Cyanobacterium Trichodesmium to a Thermally Variable Environment as a Function of Phosphorus Availability.

Surface temperature in the ocean is projected to be elevated and more variable in the future, which will interact with other environmental changes like reduced nutrient supplies. To explore these multiple stressor relationships, we tested the influence of thermal variation on the key marine diazotrophic cyanobacterium Trichodesmium erythraeum GBRTRLI101 as a function of the limiting nutrient phosphorus (P). Two constant temperature treatments represented current winter (22°C) and summer (30°C) mean values. Three variable temperature treatments fluctuated around the constant control values: Mean 22°C, either ± 2°C or ± 4°C; and mean 30°C ± 2°C. Each thermal treatment was grown under both P-replete (10 µmol/L) and P-limiting conditions (0.2 µmol/L). Effects of thermal variability on Trichodesmium were mainly found in the two winter variable temperature treatments (22°C ± 2°C or ± 4°C). P availability affected growth and physiology in all treatments and had significant interactions with temperature. P-replete cultures had higher growth and nitrogen and carbon fixation rates in the 22°C constant control, than in the corresponding variable treatments. However, physiological rates were not different in the P-replete constant and variable treatments at 30°C. In contrast, in P-limited cultures an advantage of constant temperature over variable temperature was not apparent. Phosphorus use efficiencies (PUE, mol N or C fixed h-1 mol cellular P-1) for nitrogen and carbon fixation were significantly elevated under P-limited conditions, and increased with temperature from 22 to 30°C, implying a potential advantage in a future warmer, P-limited environment. Taken together, these results imply that future increasing temperature and greater thermal variability could have significant feedback interactions with the projected intensification of P-limitation of marine N2-fixing cyanobacteria.

Jellyfish Life Stages Shape Associated Microbial Communities, While a Core Microbiome Is Maintained Across All.

The key to 650 million years of evolutionary success in jellyfish is adaptability: with alternating benthic and pelagic generations, sexual and asexual reproductive modes, multitudes of body forms and a cosmopolitan distribution, jellyfish are likely to have established a plenitude of microbial associations. Here we explored bacterial assemblages in the scyphozoan jellyfish Chrysaora plocamia (Lesson 1832). Life stages involved in propagation through cyst formation, i.e., the mother polyp, its dormant cysts (podocysts), and polyps recently excysted (excysts) from podocysts - were investigated. Associated bacterial assemblages were assessed using MiSeq Illumina paired-end tag sequencing of the V1V2 region of the 16S rRNA gene. A microbial core-community was identified as present through all investigated life stages, including bacteria with closest relatives known to be key drivers of carbon, nitrogen, phosphorus, and sulfur cycling. Moreover, the fact that half of C. plocamia's core bacteria were also present in life stages of the jellyfish Aurelia aurita, suggests that this bacterial community might represent an intrinsic characteristic of scyphozoan jellyfish, contributing to their evolutionary success.