Age polyethism drives community structure of the bacterial gut microbiota in the fungus‐cultivating termite <scp><i>O</i></scp><i>dontotermes formosanus</i>

Li, Hongjie; Dietrich, Carsten; Zhu, Na; Mikaelyan, Aram; Ma, Bin; Pi, Ruoxi; Yu, Lie; Yang, Minghan; Brune, Andreas; Mo, Jianchu

doi:10.1111/1462-2920.13046

Cited by 37 publications

(46 citation statements)

References 55 publications

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“…Lachnospiraceae are more abundant in Odontotermes formosanus young termites feeding mainly on 329 fungal nodules or degrading non-cellulosic plant oligosaccharides (Li et al, 2016) and contributing 330 to lignin depolymerisation (Li et al, 2017). Similarly, Alistipes III (OTU8, Figure 1B; 331 Supplementary Table S2) was significantly more abundant in Odontotermes soldier guts compared 332 to worker guts ( Figure 2I, J), consistent with the sequencing results ( Figure 1B, Supplementary 333 Table S12).…”

Section: Sequencing and Bacterial Identification 240supporting

confidence: 70%

Gut microbial compositions mirror caste-specific diets in a major lineage of eusocial insects

Otani

Zhukova

Koné

et al. 2018

Preprint

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25Eusocial insects owe their ecological success to the division of labour and processes within colonies 26 often rely on the presence of specific microbial symbionts, but associations between microbial 27 community compositions and castes with different tasks and diets within colonies remain largely 28 unexplored. Fungus-growing termites evolved to use fungi to externally degrade plant material, 29complemented by specific and complex gut microbiotas. Here we explore to which extent division 30 of labour and dietary differences within fungus-growing termite castes are linked to gut bacterial 31 community structure. Using amplicon sequencing, we characterise community compositions in 32 sterile (worker and soldier) and reproductive (queen and king) termites and combine this with gut 33 enzyme, microscopy, and in situ analyses to further elucidate sterile caste-specific microbiota 34 compositions. Gut bacterial communities are structured primarily according to termite caste and 35 genus. In contrast to the observed rich and diverse sterile caste microbiotas, royal pair microbiotas 36 are extremely skewed and dominated by few bacterial taxa, reflecting the specialised dietary intake 37 and unique, reproduction-centred lifestyle of the queen and king. 38 39

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Section: Sequencing and Bacterial Identification 240supporting

confidence: 70%

Gut microbial compositions mirror caste-specific diets in a major lineage of eusocial insects

Otani

Zhukova

Koné

et al. 2018

Preprint

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“…Apparently, the enzymes in young worker termite guts work in conjunction with intestinal microbiota to depolymerize lignin. Moreover, the comparative studies of fresh and middle-aged fungus comb showed that continuous cleavage of lignin sidechains is occurring throughout this process, but with no further depletion in the mature fungus comb, implying the bacterial lineages in the fresh comb derived from the feces of young workers may have similar lignin-degrading abilities to those in the gut, and thus subsequently contribute to the complete lignin depolymerization (39,40).…”

Section: Original Poplar Woodmentioning

confidence: 97%

“…microbiome-including its dense Termitomyces mycelial mass, replete with laccases, and harboring unique bacterial lineageshas the ability to extensively mineralize aromatics (39,40).…”

Section: Original Poplar Woodmentioning

confidence: 99%

Lignocellulose pretreatment in a fungus-cultivating termite

Yelle

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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Depolymerizing lignin, the complex phenolic polymer fortifying plant cell walls, is an essential but challenging starting point for the lignocellulosics industries. The variety of ether-and carbon-carbon interunit linkages produced via radical coupling during lignification limit chemical and biological depolymerization efficiency. In an ancient fungus-cultivating termite system, we reveal unprecedentedly rapid lignin depolymerization and degradation by combining laboratory feeding experiments, lignocellulosic compositional measurements, electron microscopy, 2D-NMR, and thermochemolysis. In a gut transit time of under 3.5 h, in young worker termites, poplar lignin sidechains are extensively cleaved and the polymer is significantly depleted, leaving a residue almost completely devoid of various condensed units that are traditionally recognized to be the most recalcitrant. Subsequently, the fungus-comb microbiome preferentially uses xylose and cleaves polysaccharides, thus facilitating final utilization of easily digestible oligosaccharides by old worker termites. This complementary symbiotic pretreatment process in the fungus-growing termite symbiosis reveals a previously unappreciated natural system for efficient lignocellulose degradation.ignin is a heterogeneous plant cell wall polymer derived primarily from hydroxycinnamyl alcohols via combinatorial radical coupling reactions (1). Its depolymerization is challenging, making lignin a major barrier to gaining access to stored energy within lignocellulosic materials (2). Woody biomass, such as that contained in pine and poplar trees, represents the most abundant renewable energy resource in our terrestrial ecosystems. Because of a high content of lignin, a complex polymer that contains ether-and carbon-carbon linkages between monomerderived units (1, 3), biotechnological efforts to use this material for bioenergy require expensive chemical, physical, or biological pretreatment processes to partially delignify lignocellulose to allow access to plant polysaccharides (2).Termites are remarkably efficient at degrading woody biomass (4). Within hours, they digest 74-99% of cellulose and 65-87% of hemicellulose, leaving the lignin-rich residues as feces; that is, they process far more efficiently than other herbivores that can digest the less-lignified forages, such as grasses, leaves, and forest litter (5). Among termites, the subfamily Macrotermitinae form a monophyletic group of diverse species that originated in Africa and have cultivated specialized fungi (Termitomyces spp.) in their nests using woody or litter-based biomass for about 31 million years, and are able to almost completely decompose lignocellulose (6, 7). These termites enable the consumption of more than 90% of dead plant tissues in some arid tropical areas (7,8), and thus play central ecological roles in Old World (sub)tropical carbon cycling ( Fig. 1 A and B) (8). Throughout their evolutionary history, fungus-cultivating termites have evolved in mutualistic association with multiple microbial symbi...

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“…Microbial communities differ between hosts that specialize on different substrates (Muegge et al , 2011) and changes in these communities and their functional capacity are integral to their hosts’ transition to utilizing novel substrates (Hammer and Bowers, 2015; Delsuc et al , 2013; Li et al , 2015; Kohl et al , 2014; 2016). This phenomenon is not isolated to herbivores – in many systems, gut microbial communities are influence by the inputs of their hosts (Goffredi et al , 2005; Roman et al , 2015; Muegge et al , 2011; Youngblut et al , 2019; Wang et al , 2011; Li et al , 2016).…”

Section: Introductionmentioning

confidence: 99%

Metagenomics reveals diet-specific specialization of bacterial communities in fungus gardens of grass- and dicot-cutter ants

Khadempour

Fan

Keefover‐Ring

et al. 2018

Preprint

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Leaf-cutter ants in the genus Atta are dominant herbivores in the Neotropics. While most species of Atta cut dicots to incorporate into their fungus gardens, some species specialize on grasses. Here we examine the bacterial community associated with the fungus gardens of grass- and dicot-cutter ants to examine how changes in substrate input affect the bacterial community. We sequenced the metagenomes of 12 Atta fungus gardens, across four species of ants, with a total of 5.316 Gbp of sequence data. We show significant differences in the fungus garden bacterial community composition between dicot- and grass-cutter ants, with grass-cutter ants having lower diversity. Reflecting this difference in community composition, the bacterial functional profiles between the fungus gardens are significantly different. Specifically, grass-cutter ant fungus garden metagenomes are particularly enriched for genes responsible for amino acid, siderophore, and terpenoid biosynthesis while dicot-cutter ant fungus gardens metagenomes are enriched in genes involved in membrane transport. These differences in bacterial community composition and functional capacity show that different substrate inputs matter for fungus garden bacteria, and sheds light on the potential role of bacteria in mediating the ants’ transition to the use of a novel substrate.

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Age polyethism drives community structure of the bacterial gut microbiota in the fungus‐cultivating termite Odontotermes formosanus

Cited by 37 publications

References 55 publications

Gut microbial compositions mirror caste-specific diets in a major lineage of eusocial insects

Gut microbial compositions mirror caste-specific diets in a major lineage of eusocial insects

Lignocellulose pretreatment in a fungus-cultivating termite

Metagenomics reveals diet-specific specialization of bacterial communities in fungus gardens of grass- and dicot-cutter ants

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