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Downloaded and Checked for Similarity Using Fastani bioRxiv preprint doi: https://doi.org/10.1101/2021.03.10.434842; this version posted March 11, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 1 Alphaproteobacteria facilitate Trichodesmium community 2 trimethylamine utilization 3 4 Asa E. Conovera,b, Michael Morandoa, Yiming Zhaoa, Jacob Semonesa, David A. 5 Hutchinsa, Eric A. Webba 6 7 a Department of Marine and Environmental Biology, University of Southern California, 8 California, U.S.A 9 b Department of Ecology and Evolutionary Biology, University of California Santa 10 Cruz, California, U.S.A. (current affiliation) 11 12 Correspondence 13 Eric A. Webb 14 Marine and Environmental Biology 15 Dept. of Biological Sciences at University of Southern California, AHF 137 16 3616 Trousdale Parkway 17 Los Angeles, CA 90089-0371 18 Phone: 213-740-7954 19 Email: [email protected] 20 21 Competing interests: The authors declare no competing interests. 22 Running Title: Metabolism of TMA in the Trichodesmium consortium 23 24 1 bioRxiv preprint doi: https://doi.org/10.1101/2021.03.10.434842; this version posted March 11, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 25 Originality-Significance Statement 26 Colonies and filaments of the globally-significant nitrogen-fixing cyanobacterium 27 Trichodesmium host a diverse consortium of heterotrophic bacteria. It has been 28 predicted that these bacteria support the growth of Trichodesmium by performing 29 useful metabolic functions. Herein, we provide evidence that associated microbiota 30 can metabolize the dissolved organic nitrogen compound trimethylamine, and in 31 doing so, provide Trichodesmium with a viable nitrogen source alternative to the 32 costly process of N2 fixation. The results highlight the significance of associated 33 microbiota in Trichodesmium physiology, and further implicate the microbial loop and 34 organic nitrogen supply in modulating global N2 fixation patterns. 35 36 Summary 37 In the surface waters of the warm oligotrophic ocean, filaments and 38 aggregated colonies of the nitrogen (N)-fixing cyanobacterium Trichodesmium create 39 microscale nutrient-rich oases. These hotspots fuel primary productivity and harbor a 40 diverse consortium of heterotrophs. Interactions with associated microbiota can 41 affect the physiology of Trichodesmium, often in ways that have been predicted to 42 support its growth. Recently, it was found that trimethylamine (TMA), a globally- 43 abundant organic N compound, inhibits N2 fixation in cultures of Trichodesmium 44 without impairing growth rate, suggesting that Trichodesmium receives nitrogen from 45 TMA. In this study, 15N-TMA DNA stable isotope probing (SIP) of a Trichodesmium 46 enrichment was employed to further investigate TMA metabolism and determine if 47 TMA-N is incorporated directly or secondarily via cross-feeding facilitated by 48 microbial associates. Herein we identify two members of the marine Roseobacter 49 clade (MRC) of Alphaproteobacteria as the likely metabolizers of TMA and provide 2 bioRxiv preprint doi: https://doi.org/10.1101/2021.03.10.434842; this version posted March 11, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 50 genomic evidence that they converted TMA into a more readily available form of N, + 51 e.g., NH4 , which was subsequently used by Trichodesmium and the rest of the 52 community. The results implicate microbiome-mediated carbon (C) and N 53 transformations in modulating N2 fixation, and thus highlight the involvement of host- 54 associated heterotrophs in global biogeochemical cycling. 55 56 Introduction 57 The N-fixing cyanobacterium Trichodesmium contributes a substantial portion 58 of the new nitrogen and carbon in the warm oligotrophic ocean (Capone et al., 1997; 59 Karl et al., 1997; Capone et al., 2005; Zehr and Capone, 2020). Trichodesmium 60 grows in multicell filaments called trichomes, which can aggregate to form 61 macroscopic colonies. Trichomes and colonies of Trichodesmium create micro-scale 62 nutrient hotspots, referred to as the phycosphere or trichosphere, that attract and 63 support the growth of many heterotrophic organisms (e.g., Hmelo et al., 2012; 64 Frischkorn et al., 2017; Klawonn et al., 2020; Zehr and Capone, 2020). Evidence 65 suggests that such heterotrophs may confer physiological benefits to Trichodesmium, 66 such as through drawdown of oxygen (an inhibitor of N2 fixation), production of CO2 67 (required for photosynthesis), detoxification of radical oxygen species, and 68 production of siderophores and alkaline phosphatases for acquisition of Fe and P, 69 respectively (Paerl et al., 1989; Webb et al., 2007; Hynes et al., 2009; Roe et al., 70 2012; Lee et al., 2017; Basu et al., 2019). Attempts to culture Trichodesmium 71 axenically have been challenging, though a single successful effort in the early 72 2000s by Waterbury found that axenic cultures of Trichodesmium erythraeum 73 IMS101 grow at a reduced rate (personal communication), further suggesting that 74 associated microbiota play an important role in Trichodesmium physiology. 3 bioRxiv preprint doi: https://doi.org/10.1101/2021.03.10.434842; this version posted March 11, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 75 The tight association between Trichodesmium and its heterotrophic 76 consortium has made it historically difficult to discern which metabolic functions 77 specific taxa perform and what chemical compounds mediate these interactions. 78 Recent studies have suggested that methylated amines (MAs) may play important 79 functions in Trichodesmium consortium dynamics. Pade et al. (2016) found that 80 Trichodesmium erythraeum IMS101 produces the quaternary ammonium compound 81 N,N,N-trimethyl homoserine (or homoserine betaine), a member of the methylamine 82 family, as its main compatible solute to maintain osmotic balance. Walworth et al. 83 (2018) showed that TMA, a globally-abundant organic N compound, can support 84 growth of T. erythraeum IMS101 in non-axenic culture while suppressing N2 fixation, 85 suggesting that Trichodesmium can use TMA as a N source. The latter study further 86 found that long-term growth with elevated CO2 and limiting nutrients led 87 Trichodesmium to downregulate transcription of the N2-fixing nitrogenase enzyme 88 and upregulate production of a gene predicted to encode trimethylamine 89 monooxygenase (Tmm) — an enzyme that catalyzes the oxidation of TMA to 90 trimethylamine N-oxide (TMAO), the first step in aerobic TMA catabolism (Chen et al., 91 2011; Lidbury et al., 2014; Sun et al., 2019). But while T. erythraeum IMS101 92 possesses a likely Tmm homologue, it lacks other known genes required for TMA 93 utilization (Walworth et al., 2015). It thus remains unclear if Trichodesmium is 94 capable of consuming TMA directly, or if TMA is first metabolized by associated 95 microbiota and then transferred to Trichodesmium as an alternate form of nitrogen. 96 Trichodesmium colonies have been found to host likely metabolizers of MAs. 97 Roseibium sp. TrichSKD4, a member of the marine Roseobacter clade (MRC) of 98 Alphaproteobacteria, was isolated from Trichodesmium colonies in defined media 99 and subsequently found to possess the full set of genes required for TMAO 4 bioRxiv preprint doi: https://doi.org/10.1101/2021.03.10.434842; this version posted March 11, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 100 catabolism (Lidbury, 2015). However, it lacks the tmm gene for conversion of TMA to 101 TMAO (Lidbury, 2015), suggesting potential to benefit from Trichodesmium derived 102 Tmm activity. 103 Chen et al. (2012) demonstrate that several members of the MRC can use 104 MAs, including TMA, as a sole N source, and that many have the genetic potential to 105 do so. Lidbury et al. (2015) show that TMA catabolism in MRC member Ruegeria 106 pomeroyi DSS-3 generates cellular energy and remineralizes ammonium, which 107 supports the growth of co-cultured bacteria. The production of ammonium, a known 108 N source for Trichodesmium (Mulholland and Capone, 1999), highlights a potential 109 mechanism whereby Trichodesmium may receive N through exogenous TMA 110 metabolism. However, the occurrence of such secondary utilization, and more 111 broadly, the potential influence that recycling of N compounds by heterotrophs has 112 on rates of N2 fixation, has yet to be resolved. 113 In this study, we examine whether Trichodesmium receives nitrogen from 114 TMA directly (Figure 1, Option A) or secondarily via conversion to an alternate 115 nitrogen species by a co-cultured heterotroph (Figure 1, Option B). 15N-TMA DNA 116 SIP was used to investigate TMA metabolism in non-axenic cultures of 117 Trichodesmium erythraeum GBRTRLIN201 (hereafter LIN). Our results suggest that 118 TMA catabolism by co-cultured MRC taxa has the ability to provide Trichodesmium 119 with a N source, and thereby modulate N2 fixation. 120 Results 121 As seen in Walworth et al. (2018) with T. erythraeum IMS101, the addition of 15 14 122 80 µM TMA suppressed N2 fixation by day 1 in both heavy ( N) and light ( N) 123 treatments of T. erythraeum LIN culture, reducing fixation rates to 10 - 30% that of 124 the no-addition control cultures (Figure 2, bottom panel).
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