Philippa Kaur

Many ocean sharks, including the grey reef shark, are endangered as a result of sharp declines in their numbers.Credit: Alexis Rosenfeld/Getty

The United Nations high seas treaty has been a long time coming. Secured earlier this month after almost 20 years of effort, it will be the first international law to offer some protection to the nearly two-thirds of the ocean that is beyond national control. These parts of the ocean currently have few, if any, meaningful safeguards against pollution, overfishing and habitat destruction. The treaty is without doubt a major achievement.Agreed under the UN Convention on the Law of the Sea, it represents several wins. Among them is the capacity to create marine protected areas through decisions of a conference of the parties to the treaty. It also recognizes that genetic resources of the high seas must benefit all of humanity. Moreover, companies planning commercial activities and organizations considering other large projects (such as potential climate interventions involving the ocean) will need to carry out environmental impact assessments.
UN forges historic deal to protect ocean life: what researchers think
Countries will be permitted to profit from exploiting marine genetic resources, but they must channel a proportion of their profits into a global fund to protect the high seas. Although the details are still to be worked out, high-income countries active in marine genetic research will be asked to contribute proportionately more to the fund.The treaty contains many opportunities for research in ocean science, for building research capacity in low- and middle-income countries, and for improving the evidence available to decision makers. Researchers working with marine genetic resources will need to register their interests with a central clearing house and commit to making data and research outputs open access.Scientists will have an important role in ensuring the treaty’s ultimate success. In part, this will involve gathering or improving the evidence to support the establishment and maintenance of strong marine protected areas and to inform stringent environmental impact assessments. Beyond that, researchers must make every effort to ensure transparency, including declaring the origin and prospective use of any genetic material, and making digital sequence information available through international repositories. This will not only enhance cooperation and capacity-building, but will also help governments to develop their own national regulations and procedures in line with the treaty.There’s also the potential for fresh scientific collaboration — for example, using emerging technologies such as telepresence, whereby scientists can take part in research cruises remotely. Marine scientists travelling to, say, the Pacific Ocean could collect samples under the guidance of colleagues elsewhere in real time. The knowledge gained from such collaborations could lead to the commercialization of new products, benefiting scientists and economies around the world.However, it is important not to overstate the treaty’s potential: notwithstanding its successes, there are deficiencies that the international community, supported by the research community, must now work to remedy.

Rena Lee, president of the high seas treaty conference, concluded proceedings on 3 March with the words “the ship has reached the shore”.Credit: Kena Betancur/AFP/Getty

As the planet warms, the Arctic’s permanent ice cover is melting, and China is planning a shipping route through the Central Arctic Ocean. This could become a regular passageway for shipping between Asia and Europe within a decade. In the Pacific, mining companies are exploring the deep sea bed for metals that they say are needed for the batteries that will power the coming green-energy transition. But these activities won’t face scrutiny under the treaty, because the treaty’s provisions don’t overrule regulations laid down by the authorities that oversee existing high seas activities. These include the International Maritime Organization, which is responsible for shipping; the International Seabed Authority, which oversees deep-sea mining; and some 17 regional fisheries management organizations tasked with regulating fisheries in various parts of the ocean, including Antarctica. Military activities and existing fishing and commercial shipping are, in fact, exempt from the treaty.
Protecting the ocean requires better progress metrics
This means, for example, that the treaty cannot create protected areas in places already covered by fishing agreements, even if that fishing is unsustainable and depleting stocks. This is a gaping hole. The overexploitation of coastal fisheries has made a frontier of the high seas, as fleets travel farther and fish for longer in search of dwindling resources. One outcome is that stocks of some highly migratory species, such as tuna, have dropped precipitously since the 1950s (M. J. Juan-Jordá et al. Proc. Natl Acad. Sci. USA 108, 20650–20655; 2011). By 2018, the Pacific bluefin tuna, for instance, was at 3.3% of 1952 levels (see go.nature.com/3mpimbh). Oceanic sharks and rays have also declined globally by 71% since 1970 (N. Pacoureau et al. Nature 589, 567–571; 2021). Once the treaty becomes law (after it has been ratified in the national parliaments of at least 60 countries), it can demand that proposed ocean activities — such as climate-intervention experiments — are subject to stringent environmental impact assessments. But it cannot do the same for activities already under way.Nor will the treaty end current offshore environmental violations. Farming waste, in the form of excessive nutrients, routinely ends up in rivers and coastal waters. From there, it makes its way to the open ocean, where it results in the formation of dead zones — vast areas devoid of life. Between 2008 and 2019, the number of these zones nearly doubled, from 400 to 700 (see go.nature.com/3mpigh1). So much plastic is now entering our seas that the oceans are thought to contain around 200 million tonnes. Meanwhile, cruise ships legally discharge more than one billion tonnes of raw sewage into international waters every year.Nonetheless, as humanity’s first serious attempt to challenge the carnage that prevails offshore, the high seas treaty is a triumph for diplomacy, particularly at a time when multilateralism is under sustained pressure. At present, just 1% of international waters are protected. That proportion is now set to grow, and this will help to maintain the health of our oceans and stem biodiversity loss. In securing this deal, the international community has given itself a fighting chance of coming good on earlier promises — most recently reiterated under the UN Convention on Biological Diversity — to protect 30% of the ocean by 2030.Full implementation, although some years away, offers scientists a once-in-a-generation opportunity to use their knowledge to support offshore conservation. In redressing our ‘out of sight, out of mind’ relationship with the oceans, the high seas treaty will allow us — supported by a burgeoning research effort — to rethink how we use our ocean commons in ways that benefit the majority. More

Most legislation to protect wildlife currently focuses on prohibiting deliberate destruction and excessive exploitation of resources. However, that approach fails to address emerging threats such as climate change. Many species will go extinct long before emissions-reduction schemes are realized.
Competing Interests
The authors declare no competing interests. More

In many conservation projects, women are alone on all-male teams.Credit: Getty

My career in conservation spans more than 20 countries, and workplaces ranging from universities, governments and consultancies to community-based and global non-governmental organizations (NGOs). Currently, I work as the Asia-Pacific director of gender and equity at The Nature Conservancy, one of the largest global conservation NGOs: it has more than 4,000 staff members and is active in more than 80 countries. I am responsible for ensuring that all our endeavours across the Asia-Pacific to address biodiversity loss and the climate crisis are inclusive and equitable.My career has been incredibly diverse: from monitoring saltwater crocodiles (Crocodylus porosus) in northern Australia to working with women on gender-based violence in Papua New Guinea to speaking at international climate meetings. But one theme has remained a constant: gender-based discrimination, which not only holds women back, but holds the world back from addressing the crises of climate change and biodiversity loss.Discrimination is by no means an experience unique to me or just a few women. A review of 230 peer-reviewed articles1, of which I was the lead author, confirmed a sobering truth: women everywhere are excluded from decisions about conservation and natural resources, from small and remote communities in biodiversity hotspots to large conservation organizations themselves. In every country, and in almost every setting and organization, women are routinely disadvantaged in conservation just because they are women.
Collection: Fieldwork
Unconscious bias is normal and natural, and all of us have it: it is how our brains make sense of the world. But when unexamined bias or deliberate discrimination influences decision-making, perpetuates stereotypes and keeps women from reaching their potential, they create rippling negative impacts on society and the future of our planet. Whether gender stereotypes are overtly hostile (such as ‘women are too emotional to lead fieldwork’) or seemingly benign (‘women are naturally good at organizing and supporting the team’ or ‘we need a strong, decisive leader’ — that is, a man), they hold women back in their conservation careers.An uneven playing fieldConservation has historically been a male-dominated profession. Just 3–11% of wildlife rangers are women2, and only 11% of the top-publishing authors in conservation and ecology are women3. A strong masculine culture is often associated with the profession, which can intimidate women. Many women in the sector experience sexual harassment and anxiety about their personal safety — particularly when they are the only woman on a project, which is often the case.Furthermore, women usually pay a heavy price for calling out cultures that are not inclusive. From surveying conservation professionals, I found that nearly 20% of women fear reprisal when speaking out against bias4. Their fears are warranted; many are sidelined or branded as ‘difficult’ or ‘frustrating’ if they draw attention to discrimination or poor behaviour, or try to slow down the decision-making process if it is not inclusive.In my career, I have been told that I wouldn’t be considered for an exciting project because it would be too physically demanding, be unsafe for a woman to be alone in a remote setting or require too much time away from my young family. Decisions that are made on your behalf are infuriating — and can come at both a career cost and a financial cost. Conversely, I have been offered opportunities because I have a masculine, gender-neutral name, and the people in charge assumed that I was a man before they had met me. I was then met with surprise and scepticism when I turned up and they realized that ‘Robyn James’ is a woman. I have always held my own in these situations, but the constant pressure to prove I belonged was exhausting and came at a personal cost5,6.My experiences are those of someone who holds deep and unearned privilege: I am a white cis woman with sufficient income to support my family, and I can speak and write English (the primary language of science) well. These factors increase my opportunities to contribute. Many conservationists and scientists who are women do not have those privileges. Some are also discriminated against owing to racism in a world that favours whiteness, and those who live in places where the cost of education and health care is high, wages are low and basic services such as power and Internet are intermittent face further disadvantages.As an ally and sponsor for women in conservation and science, I am determined to leverage my position to change this. I’m focused on breaking down walls and smashing the glass ceiling for women across the sector.Here are a few ways I am using the power I have to make conservation and science more inclusive. Hopefully these ideas will help others to share their solutions or to be better allies to women.Women are needed as leadersWomen who are conservation and environmental-science graduate students or are at early career stages often tell me that they don’t often see women at senior levels7, and that leaders don’t make them feel included. I am part of an informal group of women in senior positions in conservation, representing several organizations, who attend events for undergraduates and early-career professionals. We aim to share our journeys and to be visible to women who are just starting out. We model diverse leadership styles to show alternatives to masculine ‘command and control’ leadership, which these women might have more often experienced.Women routinely undersell themselves and do not apply for promotions, so we actively encourage our younger peers to apply for positions and support them by providing feedback on CVs and sharing interview techniques, for example. I am also part of a formal mentoring and sponsorship programme to support women — especially those in the lower-income countries — to navigate and excel in systems that are not designed with their success in mind. We work through issues to do with self-esteem and confidence: some women have understandably taken biased attitudes on board, and do not realize that they are worthy of progressing in their careers. I work with them to help them to understand how incredible they really are.

Conservation scientist Robyn James works with women on the Solomon Islands.Credit: Madlyn Ero

At The Nature Conservancy, we have developed a network of more than 50 women who can share their experiences and challenges in a safe supportive environment. We ensure that we work with women to address practical challenges they encounter. These efforts range from dedicated sessions on how to address gender bias in their teams and workplaces, to working through examples of how to make progress on gender equity in the field of conservation, where speaking up might clash with cultural norms or put women at risk of retaliation.Making work more inclusiveMy research with The Nature Conservancy on gender and conservation science publishing has shown that women are vastly under-represented8: less than 2% of authors were women in lower-income countries. The organization subsequently enlisted an experienced, well-published conservation scientist to work with women across the Asia-Pacific and support them in the publishing process, from developing research ideas to submitting final publications. I ensure my own published research includes authors with diverse perspectives. For example, for the three publications that were part of my PhD research1,4,8, 86% (19) of the authors are women, of which 68% (13) are first-time authors, 47% (9) are women of colour and 5 (26%) are in lower-income countries. This demonstrates that intentional efforts make a difference.Even the wording of job descriptions can exclude women. Language inherently has gendered associations, so including words such as confident, decisive, strong and outspoken in job postings has been found to attract men and deter women from applying. Many of my colleagues have felt intimidated by the tone of conservation job advertisements, which seem to be written for men. At The Nature Conservancy, we check our job descriptions and organizational plans and strategies for gendered language using a gender decoder, a tool that assesses text for masculine-coded language that could unconsciously discourage women from applying or keep women from feeling engaged with a work programme or strategy. (You can see what the decoder finds in this article here).Wherever patriarchy is deeply entrenched, men are often favoured for higher education and technical training — and women miss out. Many conservation roles have standard and mandatory educational and technical qualifications, so women are often automatically excluded from even being able to apply for a role they could otherwise be suited for.Changes in the fieldMy leadership team and I have worked to address some of the systems and processes that might inadvertently disadvantage women. For example, in the Solomon Islands, an archipelago in the south Pacific, marine conservation and research roles that require a scuba licence immediately exclude many women in the country from applying, because almost none have access to scuba training given that men are generally prioritized for training and development opportunities. In most places where The Nature Conservancy works, our employees will only ever need a mask and snorkel. Therefore, a small change in the job description means that many more women can apply. Adjusting our standard mandatory requirements has led to some fantastic women successfully applying and becoming high-performing members of our conservation teams. We now carefully omit any technical requirements that are not essential to a role or that can be easily obtained through on-the-job training.We ensure women are included in the teams that develop and implement workplace health and safety protocols, and have broadened our definition of workplace health and safety to include psychological safety and protection from gender-based violence (including sexual harassment). We worked with experienced professionals in this area to develop organization-wide guidance for our staff and partners. We also develop tailored plans depending on the country we are in to specifically address safety for women. For example, in Papua New Guinea, some women on our teams made it clear that it was unsafe for them to travel home after dark on public transport. In this country, more than two-thirds of women have experienced violence. We commissioned an official work vehicle to take staff home after hours.We ensure women have basic field equipment that is suitable for them. We provide women’s sizes in all protective gear: everything from gloves for fire protection to life jackets. This is organized before a trip or fieldwork takes place.We are also implementing protocols to ensure our conservation teams are diverse and that women are not on their own among all-male research groups. This is not only safer for women, but has repeatedly led to better conservation outcomes: the women notice things that have previously been missed. For example, in Mongolia, women in herding communities are often unable to attend important research meetings about grassland management because there is no access to toilets or because training sessions are held at times when they have caring obligations. The women on the project noticed this, and worked with the herders to ensure the infrastructure was adequate and the schedule was adjusted so that they could participate and share their unique perspectives on improving grassland conservation.Women benefit from more women being in the sector. From early-career to senior positions, representation matters. But this alone is not enough. Historically male-dominated sectors, such as conservation, that now have a relatively equal gender balance in undergraduate courses need to push for cultural change as well. This is the most difficult part of my role: challenging male leaders and systems that are not designed for women to succeed.Although we need to listen and respond to the needs of women, this is never something that should be the burden of women alone to fix. Strong leadership across our sector that prioritizes gender equity and inclusion in conservation, and provides resources to achieve it, is crucial.Women will thrive in conservation science if we keep pushing to move from equality to inclusion. Inclusion means not only that women are present, but that workplaces and programmes are designed and tailored with and for them. We shouldn’t be surprised or blame women when they don’t succeed in conservation and science workplaces and programmes that are still not actively including them. Women make up more than 50% of the population; we need to have a say in the future of our planet! More

Non-prokaryotic metagenomic sequences confound average genome size estimationsIn this work, we employed MicrobeCensus22 for de novo estimation of the average genome size (AGS) of microorganisms captured in shotgun metagenome sequences (Fig. 1a; Supplementary Data 1). Briefly, MicrobeCensus optimally aligns metagenomic reads to a set of 30 conserved single-copy gene (CSCG) families found in prokaryotes 22. Based on these mappings, the relative abundance of each CSCG is then computed and used to estimate AGS based on the proportionality principle—that is, the AGS of the community is inversely proportional to the relative abundance of each marker genes22. Finally, a weighted average AGS is calculated that excludes outliers to obtain a robust AGS estimate for a given metagenomic sample22.Fig. 1: Eukaryotic and viral metagenomic reads bias AGS estimates in marine microbial metagenomes.a Schematic workflow of procedures used for estimating AGS in metagenomic samples. AGS is estimated based directly on preprocessed high-quality metagenomic reads (AGS1) and after three iterative steps to remove potential eukaryotic reads (AGS2) and viral reads detected based on the RefSeq viral genome database (AGS3) or de novo (AGS4). See the “Methods” section for more details. b Relationship between depth and proportion of total putative eukaryotic and viral sequences in marine metagenomic collections. The blue line indicates the fitted one-tailed Spearman correlation (r), with the corresponding 95% confidence intervals for the curve indicated by grey bands. The density distribution of the estimated proportion of contaminants is shown in green, with the corresponding median values (µ) highlighted. Values in parenthesis denote the filter size range of sampled metagenomes. c The fraction of ‘contaminating’ reads is highest in the epipelagic ocean relative to other ocean depth layers. EPI Epipelagic (~3–200 m), MES Mesopelagic (200–1000 m), BAT Bathypelagic (1000–4000 m). Values in parenthesis indicate the number of metagenomes. Only the results from the Malaspina Vertical Profiles (MProfile) metagenomes are shown as they cover greater depths of the global ocean (mean 1114 m; Supplementary Data 1). d Eukaryotic and viral metagenomic sequences significantly increase AGS estimates for prokaryotic plankton in marine metagenomes. Values in parenthesis show number of metagenomes for AGS1 and AGS2. e AGS estimates decreased in most metagenomic samples (85%; n = 220) after decontamination compared to predictions directly from preprocessed metagenomes by 1–19% (n = 39). Boxplots (c–e) show the median as middle horizontal (c, d) or vertical (e) lines and interquartile ranges as boxes (whiskers extend no further than 1.5 times the interquartile ranges). Data are shown as circular symbols, while mean values are shown as white colored diamonds. Values at the top (c, d) indicate the adjusted significant P-values of the unpaired (c) and paired (d) two-sided Wilcoxon test with Benjamini-Hochberg correction. Source data are provided as a Source Data file.Full size imageOf note, the AGS of complete prokaryotic genomes increases with the cumulative number of associated phages and other mobile genetic elements37. Similarly, AGS estimates derived from metagenomic sequences of uncultured “free-living” microbes (captured in 0.1–3 µm-size filters) may also be affected by putative phage and eukaryotic microbiomes sequenced concurrently in fractionated seawater samples (see,8,22). To evaluate this possibility in our AGS predictions, we compared AGS estimates obtained directly from quality-controlled metagenomes with estimates from the same metagenomes iteratively subjected to three (de novo) decontamination procedures to filter out potential eukaryotic and viral sequence reads (Fig. 1a; see details in the “Methods” section). Overall, putatively ‘contaminating’ viral and eukaryotic reads accounted for 1% to 20% (average 7.5%) of the high-quality trimmed sequences in the four microbial metagenome collections (Fig. 1b; Supplementary Data 1). As expected, the average proportion of contaminating sequences in metagenomes from large (0.2–3.0 µm) and small (0.1–1.2 µm) size fraction filters were the highest (~11%) and lowest (~5%), respectively (Fig. 1b). In addition, the proportion of contaminating reads was significantly dependent on the depth layer of the ocean (Kruskal-Wallis χ2 = 32.40, df = 2, p  200–1000 m), and bathypelagic (BAT,  > 1000–4000 m). c AGS estimates in the “free-living” (0.2–0.8 µm) and particle-associated (0.8–20 µm) bathypelagic microbiome sampled latitudinally at 4000 m depth during the Malaspina expedition. Boxplots show the median as middle horizontal line and interquartile ranges as boxes (whiskers extend no further than 1.5 times the interquartile ranges). Data are shown as circular symbols, while mean values are shown as white colored diamonds. Values at the top indicate the adjusted significant P-values of the unpaired (b) and paired (c) two-sided Wilcoxon test with Benjamini-Hochberg correction. The number of metagenomes analyzed is indicated in parentheses in all three panels. Source data are provided as a Source Data file.Full size imageThe median AGS estimate range of 2.2 to ~3.0 Mbp in the sampled free-living (0.1–3 µm in size) marine prokaryotic communities (n = 209 metagenomes) is consistent with other large-scale metagenome sequence-based estimates and the sizes of metagenome-assembled prokaryotic genomes (MAGs; in 0.22–3 µm filters) from the photic ocean (surface to mesopelagic) based on the Tara Oceans Expedition (1.5–2.3 Mbp)15,16. Overall, our metagenome sequence-based AGS estimates support the unimodal distribution of prokaryotic genome sizes recently demonstrated in environmental genomes in several biomes38 and on cultured isolates (including marine bacterioplankton)14,39. However, estimates from isolates are likely biased since current cultivation approaches tend to favor copiotrophs (see, ref. 3).We next tested whether the derived AGS estimates depended on microbial cell size by analyzing 25 paired bathypelagic metagenomes (MDeep; Supplementary Data 1) sampled during the global Malaspina Expedition40 in which both prokaryotic life strategies, free-living (0.2–0.8 µm size) and particle-associated (0.8–20 µm size), were sampled simultaneously35. The analyzed metagenomes (MDeep) were from the Atlantic, Pacific, and Indian Ocean provinces and cover a spatial distance of 9437 km with an average depth (± SD) of 3688 ± 526 m at the tropical and subtropical latitudes (–33.55°N to 32.0788°N). These microbial metagenomes were also screened for contaminating eukaryotic and viral sequences as indicated in Fig. 1a (see details in the “Methods” section and Supplementary Data 1). The genomes of bathypelagic prokaryotes associated with marine particles (5.6 ± 0.97 Mbp) were twice as large (paired two-sided Wilcoxon test, p  3 µm) prokaryotes, respectively (Supplementary Data 3). These estimates are also consistent with those of MAGs reconstructed from the same metagenomes in the Challenger Deep (Mariana Trench)43. Overall, this reinforces the patterns of larger AGS in particle-associated compared to free-living bathypelagic prokaryotes, and larger microbial genomes in the deep ocean compared to the upper ocean.AGS patterns are not geographically constrainedExamination of the geographic patterns of AGS estimates showed that AGS distribution was independent of geographic distance in both the regional (Red Sea, Mantel statistic r = 0.01824, p = 0.2971) and global (MProfile, r = –0.01413, p = 0.7924) ocean metagenomes. Furthermore, AGS estimates in the vertically profiled global Malaspina metagenomes (MProfile, n = 81) were significantly independent of the Longhurst biogeochemical province sampled (n = 9; Kruskal-Wallis χ2 = 1.0006, df = 8, p = 0.9982; Supplementary Data 1). The lack of covariance between the patterns of AGS estimates and geographic distance or Longhurst province sampled may reflect the high connectivity of microbial communities throughout the global ocean, particularly the redistributive effects of circulation by ocean currents and other transport processes, as well as the enormous population sizes of plankton that allow dispersal constraints to be overcome44,45. This is consistent with the relatively small differences in microbial assemblages recently found in different ocean basins23,46. Another possible explanation is the effect of seasonality, which can cause selection of different taxa, resulting in the succession of microbial communities and affecting their distribution (see, ref. 47), and thus influence AGS patterns.An assessment of the relationship between AGS and measured environmental variables (Supplementary Fig. S1; Data 1)—separately for the Red Sea metagenomes (regional scale) and Malaspina Vertical Profiles metagenomes (global scale), showed that the cumulative effect of temperature, salinity, dissolved oxygen, and depth on AGS patterns was significant at both the regional scale (n = 45; Mantel statistic r = 0.1944, p = 0.0057) and the global scale (n = 81; Mantel statistic r = 0.1779, p = 1 × 10–4). This result suggests that environmental conditions are a driving force behind predicted AGS patterns in the marine microbiome. While no significant interaction effect was evident between many environmental variables (i.e., salinity, depth, oxygen, nitrate, and phosphate) in controlling AGS patterns (one-way ANOVA, p  More

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Vitamin B12 biosynthesis potential of different bacteriaB vitamins play a key role in complex marine microbial interactions as they are obligatory cofactors in various essential metabolic reactions in all living organism [13, 14, 39,40,41]. An exciting fact about B12 is that genes for synthesis of this complex cofactor have never made the transition to the eukaryotic kingdom, although it is required by both prokaryotes and eukaryotes. De novo synthesis is restricted to a minor fraction of bacteria and archaea, thus, suggesting that the ability to synthesise B12 is disproportionate to its demand in nature [1, 4]. This phenomenon can be observed in various habitats, for example in the soil microbiome, where the proportion of B12 producers is less than one tenth [8]. Similar findings have been shown for the microbiome on human skin, where only 1% of the core species are predicted to produce B12 de novo, while 39 % of the species are predicted to use B12 for metabolism [42]. In order to adequately answer this fundamental question regarding the balance between B12 availability and consumption, we should aim to better understand the synthesis potential of individual prototrophic prokaryotes.Here we present intra- and extracellular B12 concentrations of various B12 prototrophic, alphaproteobacterial strains. The concentration of intracellular B12 differs widely between the various heterotrophic bacteria examined. Converted, B12 molecules detected per cell ranged between 664 to 26,619 in the analysed bacterial cultures, including B12-provider and B12-retainer. Such strong variation in intracellular B12 concentrations have already been shown for a number of other prokaryotes, including Archaea, heterotrophic bacteria, and cyanobacteria [11, 34]. Also, in these studies, the detected intracellular B12 values differed up to three orders of magnitude and showed values similar to the ones we detected. Whether factors such as cell size, which we did not consider in our analysis, or the exact growth phase in which we took the samples had an influence on the strong variation cannot be clarified here. It is quite conceivable that different B12 requirements of the individual cells or different regulatory mechanisms of B12 synthesis played a decisive role for the intracellular B12 concentrations. Nevertheless, we can conclude that not only the genetic B12 biosynthetic potential within a microbial community is decisive, but rather which prokaryote is actually present is crucial for the availability of B12.The extracellular concentrations of B12 detected in M. algicola and P. inhibens were about 8 and 256 times lower than respective intracellular levels. For example, M. algicola secreted about 936 B12 molecules per cell, which was roughly 85 times more as detected for P. inhibens. On the basis of the detected B12 demand of T. pseudonana determined by the bioassay, we can calculate that the eukaryote requires roughly 135,000 B12 molecules per cell, if we base the limitation of cell number solely on B12 availability. Thus, it would take about 144 living M. algicola cells that release B12 to cover the requirements for the growth of one T. pseudonana cell. In fact, the bacterial cell numbers in the stationary phase of the B12-provider-diatom co-cultures were at least 110 times higher than the cell numbers of T. pseudonana. These calculations are all based on ideal laboratory conditions, with sufficient supply of inorganic nutrients and organic substrates and may differ in natural environments where viral infections or sloppy feeding can lead to cell disruption and subsequent release of intracellular B12 [43, 44]. Also, B12 requirement of T. pseudonana cells can vary under different growth conditions. For example, it has been shown that growth of T. pseudonana even with 1 pM of B12 can result in a significant change in the metabolite pool of the diatom, which in turn may have implications for the interaction with bacteria [45]. Nevertheless, our data give a first approximate insight into the interplay between B12-producers and -consumers in the world of microorganisms.Bacterial effects on the growth of T. pseudonana
Growth characteristics of T. pseudonana in co-culture show not only the obligatory provision of B12 by bacteria but also other bacterial factors that influence growth. For example, we observed that Sulfitobacter litoralis, a representative of the Roseobacter group, showed inhibitory behaviour towards the diatom. Other studies have shown that Roseobacter group isolates can produce inhibitory substances, roseobacticides, which can suppress the growth of eukaryotic phototrophs [46]. The provision of B12 leads to a promotion in growth and, at the same time, growth of the diatom is inhibited. One reason for the different growth characteristics of the diatoms observed in co-culture with different bacteria could be the adaptation to different habitats where the bacterial isolates naturally occur.In contrast to these observations, Celeribacter baekdonensis DSM 27375 significantly stimulated the growth of T. pseudonana. Even though C. baekdonensis did not provide B12 despite being synthesized, its presence in co-culture with B12 addition significantly increased the growth rate and growth yield of T. pseudonana compared to the positive control of the corresponding experimental run. In previous bacterial-diatom co-culture experiments, it has been shown that the excretion of cyclic peptides, diketopiperazines, by a bacterium, significantly increased diatom cell numbers [47]. Another plausible scenario is the synthesis and excretion of indoleacetic acid (IAA) by C. baekdonensis, which is a growth-promoting hormone for diatoms [48]. A similar effect is also conceivable for C. baekdonensis and would be exciting to explore in greater depth.A finding that appears to be overlooked in the context of our actual question is the fact that the expected bacterial cell death does not necessarily lead to the release of B12, which would promote the growth of T. pseudonana, and thus promote the interaction. Even after up to six weeks in co-culture, we cannot observe significant growth of T. pseudonana despite the presence of a bacterial B12 prototroph. This fact highlights the importance of cell lysis mechanisms in nature, for example caused by viral infections or sloppy feeding. Already today, these two natural processes are considered to play a significant role in the turnover of dissolved organic matter [44, 49,50,51] and are likely to also have a decisive influence on the release of B-vitamins in marine ecosystems [23]. Additionally, T. pseudonana is known to secret a B12 binding protein under B12 deficient conditions that has an affinity constant of 2 × 1011 M−1. This protein might help them to acquire B12 from the surroundings, when it is released through bacterial cell lysis mechanism [52]. Other phytoplankton might also have a similar strategy to scavenge B12 from the environment. When intracellular B12 is considered as a reservoir for other B12 auxotrophic microorganisms, then, for example, already 19 M. algicola cells would be sufficient to enable the growth of one T. pseudonana cell.The vital cofactor B12 is not shared by all prototrophic bacteriaAbout half of the marine phytoplankton species are B12 auxotrophs and rely on prototrophic prokaryotes to obtain this essential vitamin [1, 53]. Several co-culture experiments have confirmed that individual marine bacterial isolates, mainly Alphaproteobacteria, enable phytoplankton species to overcome their auxotrophy by providing the essential cofactor [13,14,15,16, 27, 28]. In our study we hypothesised that not all B12 prototrophs share B12 with other microorganisms and to prove that we performed individual co-culture experiments between T. pseudonana and 33 B12 prototrophic bacteria. B12 prototrophy of the bacterial isolates was confirmed by their genetic ability to synthesize B12 (Supplementary table S2) and their ability to grow in B12-free medium. The results of our study support this hypothesis, as we were able to identify one group of bacteria that enables growth of T. pseudonana by the supply of the essential cofactor, B12-providers. On the other hand, we also identified a second group of B12 prototrophic bacteria that did not support the growth of the diatom, the B12-retainers. Moreover, while categorizing them into B12-providers and B12-retainers, we observed that there are species within one genus, such as P. inhibens and P. galleciensis, in which one is a B12-provider and the other is a B12-retainer, respectively, although both of them possess the necessary genes for B12 biosynthesis. Yet, the question remains why some bacteria share the cofactor, and others, despite an obligatory interaction enforced in co-culture, do not. In the following, we describe and discuss three scenarios that we consider plausible, whereby not only one scenario has to be correct, but rather all three can take place in the B12-retainer strains that we have identified.First, biosynthesis of metabolites, such as the energetically costly B12 cofactor, are subject to intracellular regulation. Transcriptional regulation of the B12 biosynthesis pathway determines whether, and in what quantity B12 is synthesised in the cell. For example, sigma factors can alter the specificity of an RNA polymerase for a particular promoter, so that gene expression is enhanced or reduced [54]. In the case of the bacterial isolate Propionibacterium strain UF1, the riboswitch cbiMCbl was identified to regulate the gene expression of the cobA operon and thus controls B12 biosynthesis [55]. It is also known that sufficient availability of B12 can repress B12 biosynthesis gene expression in bacteria [56, 57]. In gram-negative proteobacteria as well as in cyanobacteria, for example, cobalamin (pseudocobalamin, in case of some bacteria) biosynthesis and B12 transport genes are regulated by inhibition of translation initiation, whereas in some gram-positive bacteria gene regulation proceeds by transcriptional antitermination [58]. The mechanisms described above are likely to also occur in the bacterial isolates that we tested. The large difference between the detected intracellular B12 concentrations could therefore be due to differences in gene regulation of the different bacteria and may also have had an influence on the release of B12 in the co-culture with T. pseudonana.Second, cobalamin, which we referred to here as B12 for simplicity, belongs to a group of B12-like metabolites, called cobamides. Each cobamide differs in the lower ligand attached. For example, the common cobamide, cobalamin, which is bioavailable to most microorganisms, carries 5,6-dimethylbenzimidazol (DMB) as its lower ligand, whereas pseudocobalamin synthesised by cyanobacteria in high concentrations in the ocean and being less or not bioavailable to most microorganisms, has adenine attached as its lower ligand [11, 41, 59, 60]. In general, the lower ligands of cobamides can be divided into benzimidazoles, purines, and phenols, and more than a dozen cobamides and cobamide-analogs have already been discovered [61]. However, research into the synthesis and actual diversity of cobamides, especially in marine bacteria and archaea, is still in its infancy. In our study, we were unable to detect intracellular B12 in four out of eight bacterial B12-retainer strains, although the cell counts at the time of sampling should have been sufficient for its detection. However, as is generally the case, our LC-MS analysis only targets cobalamin (B12) with its different upper ligands (adenosyl-, cyano-, methyl-, and hydroxy-cobalamin). Therefore, we cannot exclude the possibility that the here studied bacteria synthesise different cobamides, which are possibly not or less bioavailable to T. pseudonana, and not covered by our analytical measurement method. This speculation was supported by the fact that one of these four B12- retainer strains, Sulfitobacter sp. DFL-23, does not possess the DMB synthesis gene bluB and there was no intracellular B12 detected in this strain (Supplementary table S2 and Table 2). Again, it is difficult to explain this phenomenon solely depending on the presence of annotated DMB synthesis gene, as for Loktanella salsilacus DSM 16199 no bluB gene was annotated, still we detected intracellular B12 in this strain using our detection method (Supplementary table S2 and Table 2).Third, the bacteria we have identified as B12-retainer simply may not have actively released the synthesised B12 into their environment. Regardless of the importance of B12 for the vast majority of living organisms on our planet, its excretion mechanisms are to our knowledge still largely unknown. Its size of more than 1,350 Dalton does not allow sufficient diffusion through the cell membrane, which would enable microbial interactions [32]. Thus, it is likely that an unknown mechanism is required for its release. This assumption is further supported by the fact that we were able to detect intracellular B12 in four of the eight B12-retainer strains and at concentrations comparable to those detected in the B12-provider strains. In addition, we could detect intracellular B12 in P. xiamenensis, but none in its exometabolome. On the other hand, presence of extracellular B12 was detected in the exometabolome of both the provider strains examined, M. algicola and P. inhibens. Our findings show that not all bacteria share the pivotal cofactor with their environment, which has an impact on our current understanding of the marine B12 cycle and presumably in other ecosystems as well. The active exchange of B12 and thus microbial interaction plays a much smaller role than previously assumed for a relatively large number of bacteria. Consequently, for some of the B12 prototrophic bacteria within a community, it is likely that the cofactor is only released upon cell lysis.B12 production in the marine ecosystem and ecological implicationsLooking at the original source of B12 in nature, namely prototrophic bacteria and archaea, the bacteria studied here show pronounced differences between the biosynthetic potentials of the cofactors and the ability to share them with their environment. Thus, the natural source of vitamin B12 within a given ecosystem does not primarily depend on the ratio of prototrophic bacteria, but even more crucially on how much of the cofactor is synthesised by the prototrophic prokaryotes within an ecosystem and is actively released. The fact that some bacteria do not voluntarily share B12 with ambient microorganisms, significantly increases the importance of processes, such as sloppy feeding by zooplankton or virus infections [44, 49,50,51], for the release of vitamins in the marine and likely also other ecosystems.Our results also contribute to the controversially discussed question of whether B12 prototrophic bacteria live in symbiosis with phototrophic microorganisms [13, 30]. Despite numerous co-cultivation experiments demonstrating the obligatory provision of B12 by individual bacteria to phototrophic microorganisms, the decisive question of the mechanism of provision has so far been overlooked [13,14,15,16, 27, 28]. In our view, however, this question is crucial when assessing whether a symbiotic interaction is taking place. Our results support the hypothesis that a bacterial mechanism for the active release is likely to exist, as our experiments distinguish between B12-provider and B12-retainer within prototrophic bacteria. Looking at the ecological niches and the isolation sites of the two respective groups, differences can be identified. Most B12-provider strains were isolated from or discovered in association with eukaryotic microorganisms, whereas most B12-retainer strains were isolated as free-living in the ocean (Supplementary table S4). Moreover, six of the tested bacterial strains were isolated from dinoflagellates and five of them were B12-provider. Since we used a diatom as a B12 auxotrophic organism in our study, it would also be interesting to know if these B12-provider strains also provide B12 to other phytoplankton, such as dinoflagellates. Also, in this study we only studied bacteria from the alphaproteobacteria class, since a large share of them are known to be B12 prototrophs and abundant in the marine ecosystem. For future studies, it would be interesting to see if a similar pattern of B12 provisioning can be observed in bacteria from other classes. Our results indicate that the B12 prototrophy of a bacterium does not necessarily indicate a mutualistic interaction with other auxotrophic microorganisms. However, the bacterial group of B12-provider in particular seems to favour living in close proximity to other microorganisms, which is why the exchange of B12 for e.g. organic compounds can establish itself as a distinct symbiotic interaction between individual microorganisms. More

Authors and AffiliationsCenter for Evolutionary Hologenomics, Globe Institute, University of Copenhagen, Copenhagen, DenmarkMorten T. Limborg & Jacob A. RasmussenSanger Institute, Wellcome Trust Genome Campus, Hinxton, UKPhysilia Y. S. ChuaAuthorsMorten T. LimborgPhysilia Y. S. ChuaJacob A. RasmussenCorresponding authorsCorrespondence to
Morten T. Limborg or Physilia Y. S. Chua. More

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