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Pseudomonas Can Prevent the Parasitic Fungus, While Keeping the Crop Fungus Unaffected, in 2 the Gardens of Odontotermes Obesus

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Pseudomonas Can Prevent the Parasitic Fungus, While Keeping the Crop Fungus Unaffected, in 2 the Gardens of Odontotermes Obesus bioRxiv preprint doi: https://doi.org/10.1101/2021.01.29.428757; this version posted February 19, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 1 Pseudomonas can prevent the parasitic fungus, while keeping the crop fungus unaffected, in 2 the gardens of Odontotermes obesus. 3 Renuka Agarwal1, Manisha Gupta1, Abin Antony1, Ruchira Sen2, Rhitoban Raychoudhury1* 4 5 6 1- Department of Biological Sciences, Indian Institute of Science and Education Research Mohali 7 (IISER Mohali). Knowledge City, Sector 81, SAS Nagar, Manauli PO 140306, Punjab, India. 8 2- Sri Guru Gobind Singh College, Sector 26, Chandigarh 160019, India. 9 * Corresponding Author: [email protected] 10 11 12 13 Keywords: symbiosis, Termitomyces, Pseudoxylaria, bacteria, pan-microbiome, core-microbiome 14 15 16 17 18 19 20 21 22 23 bioRxiv preprint doi: https://doi.org/10.1101/2021.01.29.428757; this version posted February 19, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 24 Abstract 25 Insects that farm monocultures of fungi are canonical examples of nutritional symbiosis as well as 26 independent evolution of agriculture in non-human animals. But just like in human agriculture, 27 these fungal crops face constant threat of invasion by weeds which, if unchecked, takes over the 28 crop fungus. In fungus-growing termites, the crop fungus (Termitomyces) faces such challenges 29 from the parasitic fungus Pseudoxylaria. The mechanism by which Pseudoxylaria is suppressed 30 is not known. However, evidence suggests that some bacterial secondary symbionts can serve as 31 defensive mutualists by preventing the growth of Pseudoxylaria. However, such secondary 32 symbionts must possess the dual, yet contrasting, capabilities of suppressing the weedy fungus 33 while keeping the growth of the crop fungus unaffected. This study describes the isolation, 34 identification and culture-dependent estimation of the roles of several such putative defensive 35 mutualists from the colonies of the wide-spread fungus-growing termite from 36 India, Odontotermes obesus. From the 38 bacterial cultures tested, a strain of Pseudomonas 37 showed significantly greater suppression of the weedy fungus than the crop fungus. Moreover, a 38 16S rRNA pan-microbiome survey, using the Nanopore platform, revealed Pseudomonas to be a 39 part of the core microbiota of Odontotermes obesus. A meta-analysis of microbiota composition 40 across different species of Odontotermes also confirms the wide-spread prevalence 41 of Pseudomonas within this termite. These evidence indicate that Pseudomonas could be playing 42 the role of defensive mutualist within Odontotermes. 43 Introduction 44 Domestication of specific fungal cultivars by insects, for food, has evolved independently over the 45 past 50 million years in three major insect lineages of ants, termites, and beetles [1-3]. Curiously, 46 fungus-growing ants and termites show parallel symbiotic evolution in two distinct geographical 47 locations. The former is found in the new world, whereas, the latter (Subfamily: Macrotermitinae) 48 are found in tropical Africa and Asia [4]. However, both systems face the invasion of parasitic 49 fungi taking over their crop. In fungus-growing termites, the most prominent of these parasites is 50 Pseudoxylaria (Phylum: Ascomycota) which invade the monoculture of the crop fungus, 51 Termitomyces (Phylum: Basidiomycota) [2, 5-7]. Termites have been reported to regulate this 52 invasion by actively grooming out any unwanted spores [8], selectively burying the parasitic fungi bioRxiv preprint doi: https://doi.org/10.1101/2021.01.29.428757; this version posted February 19, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 53 [9] and applying chemical secretions with specific anti-fungal properties [10]. However, the 54 effectiveness of these measures in controlling Pseudoxylaria remains unknown [4, 11]. 55 The presence of fungicide-producing mutualistic microbes in fungus-growing ants, which 56 arguably suppresses the growth of parasitic fungi in their colonies [12-15], points to a similar role 57 of secondary bacterial symbionts in fungus-growing termites as well [16, 17]. This conjecture is 58 strengthened by the fact that even after cultivating very divergent crop fungi, the microbiota across 59 all insect-fungal systems shows a remarkable phylogenetic and compositional similarity [18, 19]. 60 This multi-level convergent evolution suggests the importance of such secondary microbes in 61 maintaining successful nutritional symbiosis across all fungus-growing insects [18, 19]. The 62 evolutionary logic for the presence of such mutualistic microbes within these symbioses is 63 inescapable. Since, the termites cannot subsist on any fungi other than Termitomyces [20, 21] and 64 Pseudoxylaria has been found in almost all fungus-growing termites [22], colonies with such 65 mutualistic microbes would have a strong selective advantage. Consequently, many strains of 66 Bacillus and Streptomyces have been found from termite colonies which can act against 67 Pseudoxylaria [11, 23-26]. But, most of these strains also inhibit the growth of the cultivar fungus 68 [23, 24]. 69 This indicates that such a secondary symbiont cannot be a generic anti-fungal agent as it will also 70 adversely affect the crop fungus on which the termites subsist. Thus, a potential mutualist must 71 have the dual, but contrasting, capability of acting as an antagonist towards Pseudoxylaria, but, as 72 a mutualist towards Termitomyces. Unfortunately, there is no clear and unambiguous evidence of 73 such a microbe from fungus-growing termites. Moreover, the presence of such microbes has not 74 been demonstrated across the core microbiota of individual termite populations as these surveys 75 are either from the gut or from the comb [11, 27]. But if these mutualists are indeed essential then 76 they must be present within the different castes as well as the fungus comb of the termite. This is 77 especially true for winged reproductives (alates) which are the mobile castes of termites that move 78 out of the natal colony to find new ones. Alates are presumed to be equipped with the full 79 complement of the microbiota required for the successful establishment of new colonies and would 80 be selected against if they lack such critical secondary mutualists [28, 29]. Thus, the presence of 81 any such a secondary symbiont should permeate across the different castes as well as the comb. 82 However, since no such analysis of caste-specific microbiota has been reported from any fungus- bioRxiv preprint doi: https://doi.org/10.1101/2021.01.29.428757; this version posted February 19, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 83 growing termites, it is not possible to ascertain whether the previously reported microbes are an 84 essential part of the symbiosis. 85 In this study, we present evidence of the presence of several potential mutualistic bacteria within 86 the core microbial community of the fungus-growing termite Odontotermes obesus. We isolated 87 38 different bacterial cultures from different castes and the comb and tested their potential to be 88 an antagonist towards Pseudoxylaria. Then we tested some of these antagonists to ascertain 89 whether they also impede the growth of the crop fungus. A particular strain of Pseudomonas 90 appears from these two contrasting screens to be an ideal mutualist as it strongly impedes the 91 growth of Pseudoxylaria but show almost negligible inhibition of Termitomyces. To test whether 92 Pseudomonas is a part of the symbiotic community, we also enumerated the pan-microbiome of 93 O. obesus by obtaining Nanopore reads of 16S rRNA gene fragments (V3-V4 regions) from six 94 different samples (comb, both male and female alates, both major and minor workers and nymphal 95 castes). From this pan-microbiome, we then established the presence of Pseudomonas within the 96 core microbiota of O. obesus. Finally, we performed a meta-analysis of microbiota across many 97 different Odontotermes sp. and ascertain the ubiquity Pseudomonas in this termite genus. 98 Materials and Methods 99 Source of termites, combs and their DNA extraction 100 Different castes, nymphs and fungus combs of O. obesus were collected from two different 101 mounds of the IISER Mohali campus (Fig. S1-S3). The combs were collected in sterile plastic 102 bags, termites were removed and then crushed within them. These were divided into 0.5 g portions 103 in sterile glass containers. To minimize environmental contamination and degradation, DNA was 104 extracted from some of these portions within 3 hours of the collection while others were used for 105 microbial isolation. Major workers, minor workers and nymphs collected from these combs were 106 also kept in separate sterile vials. Male and female alates were collected during swarming, which 107 began after the first rains during June 2018. DNA was extracted from individual termite using the 108 CTAB (Cetyl Trimethyl Ammonium Bromide) method [30] (supplementary methods S1). 109 DNA extractions from fungus combs often have extensive humic
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